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

Vila‐Aiub, Martin M.; Yu, Qin; Powles, Stephen B.

doi:10.1111/nph.15733

Cited by 58 publications

(85 citation statements)

References 175 publications

(316 reference statements)

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“…The absence of a remarkable fitness penalty in B. subalternans double mutant plants remains to be proven but it could be different from TIPS in E. indica due to the presence of Thr106 instead of Ser106. However, mutations at Pro106 typically cause only small structural changes in the EPSPS active site of bacteria and plants . Similar K m values for phosphoenolpyruvate (PEP) are reported for TIPS and TIPT double mutations in maize .…”

Section: Resultsmentioning

confidence: 76%

“…However, mutations at Pro106 typically cause only small structural changes in the EPSPS active site of bacteria and plants. 42 Similar K m values for phosphoenolpyruvate (PEP) are reported for TIPS and TIPT double mutations in maize. 32 Furthermore, novel mutations outside the sequenced region in our research could affect substrate binding affinity with EPSPS and perhaps compensate for the lack of fitness.…”

Section: Discussionmentioning

confidence: 75%

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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: Resultsmentioning

confidence: 76%

Section: Discussionmentioning

confidence: 75%

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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“…This target‐site mutation has not been reported previously in horseweed populations in the United States (Nol, Tsikou, Eid, Livieratos, & Giannopolitis, ) or China (Mei et al, ), but it is known to occur in Ontario, Canada, where GR horseweed was first documented in 2010 (Page et al, ). We hypothesize, and the latest review by Vila‐Aiub, Yu, and Powles () suggests, that different mechanisms of glyphosate resistance, such as point mutations, EPSPS gene amplification, and vacuolar sequestration, may have different fitness effects in the absence of glyphosate in horseweed and other species. In the current study, we did not attempt to identify specific resistance mechanisms in the sampled horseweed biotypes and this would be a fruitful avenue for further research.…”

Section: Discussionmentioning

confidence: 91%

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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“…The replicon not only provides a unique heritable unit enabling adaption to herbicide stress, but also adds another 58 putative genes (aside from EPSPS ) and gene products which could conceivably alter the genomic trajectory of this species. Glyphosate resistance has not negatively impacted A. palmeri fitness [8-10] and the additional 41 expressed genes may provide advantages in areas such as abiotic and biotic stress tolerance [11]. Replicon-based glyphosate resistance represents a natural, molecular solution constructed, modified and initiated by A. palmeri , a consequence that may inform future efforts in biomolecular engineering of genes that promote survival and genomic success.…”

Section: Resultsmentioning

confidence: 99%

“…GR biotypes of A. palmeri typically contained between 40 and 100 copies of the EPSPS gene per genome equivalent [3-7] which increased the C-value of the genome by up to 11% in resistant plants [5]. Interestingly, glyphosate resistance by copy number variation and increased genome size does not seem to lead to immediate consequences to overall fitness [8-10]. The long-term evolutionary consequences of increases in DNA content from targeted amplifications are unknown and may be largely dependent on the level of expression inherited by future generations.…”

Section: Introductionmentioning

confidence: 99%

Homogeneity among glyphosate-resistantAmaranthus palmeriin geographically distant locations

Molin

Patterson

Saski

2020

Preprint

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14Since the initial report of glyphosate-resistant (GR) Amaranthus palmeri (S) Wats. in 2006, 15 resistant populations have been reported in 28 states. The mechanism of resistance is 16 amplification of a 399-kb extrachromosomal circular DNA, called the EPSPS replicon, and is 17 unique to glyphosate-resistant plants. The replicon contains a single copy of the 10-kb 5-18 enolpyruvylshikimate-3-phosphate synthase (EPSPS) gene which causes the concomitant 19 increased expression of EPSP synthase, the target enzyme of glyphosate. It is not known 20 whether the resistance by this amplification mechanism evolved once and then spread across the 21 country or evolved independently in several locations. To compare genomic representation and 22 variation across the EPSPS replicon, whole genome shotgun sequencing (WGS) and mapping of 23 sequences from both GR and susceptible (GS) biotypes to the replicon consensus sequence was 24 performed. Sampling of GR biotypes from AZ, KS, GA, MD and DE and GS biotypes from AZ, 25 KS and GA revealed complete contiguity and deep representation with sequences from GR 26 plants, but lack of homogeneity and contiguity with breaks in coverage were observed with 27 sequences from GS biotypes. The high sequence conservation among GR biotypes with very few 28 polymorphisms which were widely distributed across the USA further supports the hypothesis 29 that glyphosate resistance most likely originated from a single population. We show that the 30 replicon from different populations was unique to GR plants and had similar levels of 31 amplification. 32 33 Amaranthus palmeri, replicon 35In 2006, glyphosate resistant (GR) A. palmeri (S. Wats.) was reported in Georgia (GA) 36 [1], and since then, glyphosate-resistant populations have spread to 27 other states as far west as 37 California, and as far north as Maryland (MD) and Wisconsin [2]. The resistance mechanism in 38 A. palmeri was identified as amplification and seemingly random insertion of the 5-39 enolpyruvylshikimate-3-phosphate synthase (EPSPS) gene into the genome [3]. EPSPS gene 40 sequences from GR and GS plants were identical indicating the resistance was not due to a point 41 mutation. GR biotypes of A. palmeri typically contained between 40 and 100 copies of the 42 EPSPS gene per genome equivalent [3-7] which increased the C-value of the genome by up to 43 11% in resistant plants [5]. Interestingly, glyphosate resistance by copy number variation and 44 increased genome size does not seem to lead to immediate consequences to overall fitness [8-45 10]. The long-term evolutionary consequences of increases in DNA content from targeted 46 amplifications are unknown and may be largely dependent on the level of expression inherited by 47 future generations. 48 Previous work demonstrated that the amplified EPSPS gene was part of a co-amplified 49 297-kb sequence, the so-called the EPSPS cassette [5]. Polymerase chain reaction products from 50 40 primer pairs distributed equidistantly along this amplified, 297-kb sequence were nea...

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

Cited by 58 publications

References 175 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

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

Homogeneity among glyphosate-resistantAmaranthus palmeriin geographically distant locations

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