Scientific data published by a peer‐reviewed journal should be properly interpreted: a reply to the letter by Gressel <i>et al</i>. (2014)

Lu, Bing-Rui; Snow, Allison A.; Yang, Xiao; Wang, Wei

doi:10.1111/nph.12684

Cited by 5 publications

(9 citation statements)

References 21 publications

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“…If the lack of fitness costs associated with gene amplification/overexpression contradicts the expected metabolic cost (see Costs imposed by increased energy requirements for gene amplification/overexpression), an increase in plant fitness due to protein overproduction would probably demand a reformulation of theoretical paradigms, as suggested by recent reports on the fitness effects of a glyphosate resistance EPSPS rice transgene introgressed into weedy ( Oryza sativa f. spontanea ) and wild rice ( Oryza rufipogon ) (Lu et al ., ; Wang et al ., ; Yang et al ., ).…”

Section: Does Glyphosate Resistance By Epsps Gene Amplification and Omentioning

confidence: 99%

“…A modified native EPSPS gene (EP3) from rice, under the control of the maize ubiquitin promoter, was introgressed into various weedy rice accessions. Transgenic F 2 crop‐weed plants exhibited glyphosate resistance due to a two‐fold higher EPSPS expression and 5–25% more EPSPS protein (Lu et al ., ; Wang et al ., ). As expected, a significant increase (20–100%) in free cellular Trp concentrations was observed in transgenic compared with nontransgenic F 3 plants (Wang et al ., ).…”

Section: Does Glyphosate Resistance By Epsps Gene Amplification and Omentioning

confidence: 99%

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Do plants pay a fitness cost to be resistant to glyphosate?

Vila‐Aiub

Powles

2019

New Phytologist

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Summary We reviewed the literature to understand the effects of glyphosate resistance on plant fitness at the molecular, biochemical and physiological levels. A number of correlations between enzyme characteristics and glyphosate resistance imply the existence of a plant fitness cost associated with resistance‐conferring mutations in the glyphosate target enzyme, 5‐enolpyruvylshikimate‐3‐phosphate synthase (EPSPS). These biochemical changes result in a tradeoff between the glyphosate resistance of the EPSPS enzyme and its catalytic activity. Mutations that endow the highest resistance are more likely to decrease catalytic activity by reducing the affinity of EPSPS for its natural substrate, and/or slowing the velocity of the enzyme reaction, and are thus very likely to endow a substantial plant fitness cost. Prediction of fitness costs associated with EPSPS gene amplification and overexpression can be more problematic. The validity of cost prediction based on the theory of evolution of gene expression and resource allocation has been cast into doubt by contradictory experimental evidence. Further research providing insights into the role of the EPSPS cassette in weed adaptation, and estimations of the energy budget involved in EPSPS amplification and overexpression are required to understand and predict the biochemical and physiological bases of the fitness cost of glyphosate resistance.

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Section: Does Glyphosate Resistance By Epsps Gene Amplification and Omentioning

confidence: 99%

Section: Does Glyphosate Resistance By Epsps Gene Amplification and Omentioning

confidence: 99%

Do plants pay a fitness cost to be resistant to glyphosate?

Vila‐Aiub

Powles

2019

New Phytologist

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“…In this system, transgenic over-expression of a native EPSPS gene from cultivated rice was associated with increased seed germination, tryptophan concentrations, photosynthetic rates, and seed production in F2 and F3 crop-weed hybrids from several weedy accessions [26]. However, it is difficult to generalize from Wang et al [26] because our experimental design involved a single transgenic event rather than multiple, independent transgenic lines, and therefore it is not possible to exclude effects of the transgene insertion or linked genes [30,31]. …”

Section: Introductionmentioning

confidence: 99%

Effects of over-expressing a native gene encoding 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) on glyphosate resistance in Arabidopsis thaliana

et al. 2017

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Widespread overuse of the herbicide glyphosate, the active ingredient in RoundUp®, has led to the evolution of glyphosate-resistant weed biotypes, some of which persist by overproducing the herbicide’s target enzyme, 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS). EPSPS is a key enzyme in the shikimic acid pathway for biosynthesis of aromatic amino acids, lignin, and defensive compounds, but little is known about how overproducing EPSPS affects downstream metabolites, growth, or lifetime fitness in the absence of glyphosate. We are using Arabidopsis as a model system for investigating phenotypic effects of overproducing EPSPS, thereby avoiding confounding effects of genetic background or other mechanisms of herbicide resistance in agricultural weeds. Here, we report results from the first stage of this project. We designed a binary vector expressing a native EPSPS gene from Arabidopsis under control of the CaMV35S promoter (labelled OX, for over-expression). For both OX and the empty vector (labelled EV), we obtained nine independent T3 lines. Subsets of these lines were used to characterize glyphosate resistance in greenhouse experiments. Seven of the nine OX lines exhibited enhanced glyphosate resistance when compared to EV and wild-type control lines, and one of these was discarded due to severe deformities. The remaining six OX lines exhibited enhanced EPSPS gene expression and glyphosate resistance compared to controls. Glyphosate resistance was correlated with the degree of EPSPS over-expression for both vegetative and flowering plants, indicating that glyphosate resistance can be used as a surrogate for EPSPS expression levels in this system. These findings set the stage for examination of the effects of EPSPS over-expression on fitness-related traits in the absence of glyphosate. We invite other investigators to contact us if they wish to study gene expression, downstream metabolic effects, and other questions with these particular lines.

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“…In agreement with Grunewald and Bury, we note that the best way to test our hypothesis would have been to study crop–weed progeny derived from two or more insertion events for the transgene, but we were not able to carry out these studies due to various limitations (see Lu et al ., ). For any study of a single transgenic event, a combination of insertion‐site changes and tissue culture‐induced changes could result in heritable phenotypic effects that are independent of the transgene and may exhibit abnormal phenotypes (e.g.…”

mentioning

confidence: 97%

“…To review, our two crop parental rice lines (Fig. ) were the inbred line Minghui‐86 and a transgenic rice line (EP3), which was obtained by transforming Minghui‐86 (Su et al ., ; Lu et al ., (this issue of New Phytologist , pp. 363–366); Wang et al ., ).…”

mentioning

confidence: 99%

Using a single transgenic event to infer fitness effects in crop–weed hybrids: a reply to the Letter by Grunewald & Bury (2014)

Snow

Yang

et al. 2014

New Phytologist

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Using a single transgenic event to infer fitness effects in crop-weed hybrids: a reply to the Letter by Grunewald & Bury (2014) Grunewald & Bury (2014; in this issue of New Phytologist, pp. 367-369) criticize our recent peer-reviewed paper (Wang et al., 2014; in this issue of New Phytologist, pp. 679-683), stating that we 'unnecessarily harm the sensitive debate on GM crops.' We will not focus on this politically charged topic here, but we do want to address scientific questions about our study of transgenic cropweed (Oryza sativa and O. sativa f. spontanea) hybrids of rice. Grunewald and Bury propose that an insertion effect that stimulated tiller formation in the EP3 crop parent of these hybrids offers a more convincing explanation of our results than direct effects of a transgene for over-expressing 5-enolpyruvoylshikimate-3-phosphate synthase (epsps) (our central hypothesis). In our study, the genetically engineered (GE) segregants had significantly greater expression of epsps and produced significantly greater amounts of the enzyme of EPSPS than the non-GE segregants, as expected (Wang et al., 2014). As discussed later, we doubt that an insertion effect could account for the clear and significant increases in our transgenic lines in terms of enhanced fecundity, greater tryptophan concentrations in leaves, and other traits, which are more parsimoniously explained by transgenic over-expression of epsps and its key role in the shikimic acid pathway (Wang et al., 2014). Tryptophan is produced by this pathway and is a precursor of growth hormones (auxin) and secondary metabolites that play a role in plant defense (e.g. Maeda & Dudareva, 2012). Tryptophan is just one of many products of the shikimic acid pathway, which can account for as much as 35% of a plant's biomass (e.g. Franz et al., 1997).To review, our two crop parental rice lines (Fig. 1) were the inbred line Minghui-86 and a transgenic rice line (EP3), which was obtained by transforming Minghui-86 (Su et al., 2008; Lu et al., 2014 (this issue of New Phytologist, pp. 363-366); Wang et al., 2014). Thus, these lines differed only in the absence or presence of a single-copy insertion of the transgenic construct and possible unknown side-effects of transformation. Su et al. (2008) and our Supporting Information Table S1 (Wang et al., 2014) showed that EP3 produced significantly more tillers and panicles per plant than Minghui-86. This suggests a direct effect of the transgene on plant growth and reproduction in EP3. We do not understand why Grunewald and Bury do not even acknowledge this explanation under 'option (2)' of their letter. Instead, they assume that the superior performance of EP3 was due to a linked sequence that

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Scientific data published by a peer‐reviewed journal should be properly interpreted: a reply to the letter by Gressel et al. (2014)

Cited by 5 publications

References 21 publications

Do plants pay a fitness cost to be resistant to glyphosate?

Do plants pay a fitness cost to be resistant to glyphosate?

Effects of over-expressing a native gene encoding 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) on glyphosate resistance in Arabidopsis thaliana

Using a single transgenic event to infer fitness effects in crop–weed hybrids: a reply to the Letter by Grunewald & Bury (2014)

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