Limited fitness costs of herbicide‐resistance traits in <scp><i>Amaranthus tuberculatus</i></scp> facilitate resistance evolution

Wu, Changgong; Davis, Adam S.; Tranel, Patrick J.

doi:10.1002/ps.4706

Cited by 43 publications

(71 citation statements)

References 53 publications

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“…As outlined earlier, glyphosate resistance‐endowing amino acid substitutions at Pro‐106 lead only to low‐level glyphosate resistance and a lack of significant changes in EPSPS functionality (Table ). Not surprisingly, Pro‐106 substitutions are the most common form of target‐site glyphosate resistance (Powles & Yu, ; Sammons & Gaines, ; Morran et al ., ), and resistant individuals show no fitness cost at the plant level, and persist in populations in the absence of glyphosate selection (Yu et al ., ; Fernández‐Moreno et al ., ; Han et al ., ; Wu et al ., ).…”

Section: Do Epsps Target‐site Glyphosate Resistance Mutations Lead Tomentioning

confidence: 97%

“…Although it is reasonable to expect that the process of natural selection could have minimized the costs associated with EPSPS gene amplification (Andersson, ; Paris et al ., ; Darmency et al ., ), studies conducted over a single plant generation may not detect subtle fitness differences (Giacomini et al ., ; Vila‐Aiub et al ., ; Kumar & Jha, ; Martin et al ., ) which only manifest themselves after several generations of additive fitness cost effects (each of which could also slowly reduce the frequency of plants carrying the amplified gene) (Vila‐Aiub et al ., , , ). For instance, the frequency of A. tuberculatus plants with up to five EPSPS gene copies grown in competition decreased from 50% to less than 5% after six generations without glyphosate treatment (Wu et al ., ). Multigenerational studies rely on the fact that a costly resistance allele will decrease in frequency over time, so any significant deviations from expected resistance genotypic frequencies provide clear evidence of the expression and magnitude of a fitness cost (Roux et al ., ).…”

Section: Does Glyphosate Resistance By Epsps Gene Amplification and Omentioning

confidence: 97%

“…Based on the evolution of gene expression and resource allocation theory (reviewed in Herms & Mattson, ; Bergelson & Purrington, ; Lynch & Marinov, ), EPSPS gene amplification or overexpression should attract plant fitness penalties due to a metabolic cost. Some empirical evidence has validated this hypothesis, showing that evolved overproduction of EPSPS and downstream products incurs a fitness cost (Cockerton, ; Yanniccari et al ., ; Martin et al ., ; Wu et al ., ). However, the basis of this constrained energy budget under EPSPS amplification has been challenged, not only by those cases in which a cost has not been detectable (Giacomini et al ., ; Vila‐Aiub et al ., ; Kumar & Jha, ; Martin et al ., ; Osipitan & Dille, ), but also in those studies reporting on a fitness advantage endowed by EPSPS overexpression in transgenic plants (Lu et al ., ,b; Wang et al ., ; Yang et al ., ; Beres et al ., ; Fang et al ., ).…”

Section: Final Remarksmentioning

confidence: 97%

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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: Do Epsps Target‐site Glyphosate Resistance Mutations Lead Tomentioning

confidence: 97%

Section: Does Glyphosate Resistance By Epsps Gene Amplification and Omentioning

confidence: 97%

Section: Final Remarksmentioning

confidence: 97%

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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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“…Although diversified herbicide rotations can reduce the risk of resistance and help steward herbicides, they are mainly effective for addressing target‐site based resistance and not non‐target site resistance, e.g. through enhanced metabolic detoxification . Metabolism‐based resistance can confer resistance to unrelated herbicide SOA, thus making herbicide diversity an inadequate management approach.…”

Section: Law 5: Resources Are Finitementioning

confidence: 99%

An ecological perspective on managing weeds during the great selection for herbicide resistance

Bagavathiannan

Davis

2018

Pest Management Science

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More than 70 years after modern agriculture declared a 'war on weeds', they continue to thrive and suppress crop yields. Viewing weeds as an enemy that can be defeated if only a powerful enough technology can be deployed is a losing proposition. The latest evidence for the inadequacy of this approach, rampant evolution of multiple herbicide-resistant weed genotypes and dwindling options for chemical control in many production systems, should be seen as an urgent message to all those concerned with the science and practice of weed management: we need another way of thinking about the weed resistance issue. Fortunately, the theoretical and practical foundation of this alternative approach, ecological weed management, has been in development for decades. Here, we use Barry Commoner's laws of ecology as a conceptual frame for a review of some of the fundamental concepts of ecological weed management. © 2018 Society of Chemical Industry.

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“…Fitness‐related costs of glyphosate resistance also have been reported in glyphosate‐resistant populations of perennial ryegrass ( Lolium perenne L.) and morning glory ( Ipomoea purpurea ; Yaniccari, Vila‐Aiub, Istilart, Acciaresi, & Castro, ; Debban, Okum, Pieper, Wilson, & Baucom, ). Another study by Wu, Davis, and Tranel () found fitness costs associated with one mechanism of glyphosate resistance (EPSPS, EC2.5.1.19, gene amplification) but not for others in greenhouse‐grown, synthetic populations of Amaranthus tuberculatus . However, two well‐designed studies found no fitness costs associated with glyphosate resistance in Palmer amaranth ( Amaranthus palmeri ), a major problem weed in US agriculture (Giacomini, Westra, & Ward, ; Vila‐Aiub et al, ).…”

Section: Introductionmentioning

confidence: 99%

No evidence for early fitness penalty in glyphosate‐resistant biotypes of Conyza canadensis: Common garden experiments in the absence of glyphosate

Beres

Owen

Snow

2019

Ecology and Evolution

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Strong selection from herbicides has led to the rapid evolution of herbicide‐resistant weeds, greatly complicating weed management efforts worldwide. In particular, overreliance on glyphosate, the active ingredient in RoundUp®, has spurred the evolution of resistance to this herbicide in ≥40 species. Previously, we reported that Conyza canadensis (horseweed) has evolved extreme resistance to glyphosate, surviving at 40× the original 1× effective dosage. Here, we tested for underlying fitness effects of glyphosate resistance to better understand whether resistance could persist indefinitely in this self‐pollinating, annual weed. We sampled seeds from a single maternal plant (“biotype”) at each of 26 horseweed populations in Iowa, representing nine susceptible biotypes (S), eight with low‐level resistance (LR), and nine with extreme resistance (ER). In 2016 and 2017, we compared early growth rates and bolting dates of these biotypes in common garden experiments at two sites near Ames, Iowa. Nested ANOVAs showed that, as a group, ER biotypes attained similar or larger rosette size after 6 weeks compared to S or LR biotypes, which were similar to each other in size. Also, ER biotypes bolted 1–2 weeks earlier than S or LR biotypes. These fitness‐related traits also varied among biotypes within the same resistance category, and time to bolting was inversely correlated with rosette size across all biotypes. Disease symptoms affected 40% of all plants in 2016 and 78% in 2017, so we did not attempt to measure lifetime fecundity. In both years, the frequency of disease symptoms was greatest in S biotypes and similar in LR versus ER biotypes. Overall, our findings indicate there are no early growth penalty and possibly no lifetime fitness penalty associated with glyphosate resistance, including extremely strong resistance. We conclude that glyphosate resistance is likely to persist in horseweed populations, with or without continued selection pressure from exposure to glyphosate.

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Limited fitness costs of herbicide‐resistance traits in Amaranthus tuberculatus facilitate resistance evolution

Abstract: Our results indicate that herbicide-resistance mitigation strategies (e.g. herbicide rotation) that rely on the existence of fitness costs in the absence of herbicide selection likely will be largely ineffective in many cases. © 2017 Society of Chemical Industry.

Cited by 43 publications

References 53 publications

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

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

An ecological perspective on managing weeds during the great selection for herbicide resistance

No evidence for early fitness penalty in glyphosate‐resistant biotypes of Conyza canadensis: Common garden experiments in the absence of glyphosate

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