Metabolic Profiling and Enzyme Analyses Indicate a Potential Role of Antioxidant Systems in Complementing Glyphosate Resistance in an <i>Amaranthus palmeri</i> Biotype

Maroli, Amith S.; Nandula, Vijay K.; Dayan, Franck E.; Duke, Stephen O.; Gerard, Patrick; Tharayil, Nishanth

doi:10.1021/acs.jafc.5b04223

Cited by 65 publications

(125 citation statements)

References 53 publications

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“…In particular, in untreated plants, the level of free AAA content was similar in GR and GS populations ( Figure 5 ). Similar AAA content in glyphosate resistant/sensitive biotypes has been previously described ( Maroli et al, 2015 ). This is consistent with previous reports suggesting that the overexpression of EPSPS may have no fitness cost in A. palmeri ( Giacomini et al, 2014 ; Vila-Aiub et al, 2014 ).…”

Section: Discussionsupporting

confidence: 83%

“…PAL activity was carried out according to Orcaray et al (2011) with the following modifications. Samples were immediately centrifuged after extraction (12,000 g , 5 min) The reaction was started by the addition of 25 mM L -phenylalanine ( Maroli et al, 2015 ). Controls (without L -phenylalanine) were prepared to determine endogenous levels of transcinnamic acid (t-CA).…”

Section: Methodsmentioning

confidence: 99%

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Effects of EPSPS Copy Number Variation (CNV) and Glyphosate Application on the Aromatic and Branched Chain Amino Acid Synthesis Pathways in Amaranthus palmeri

et al. 2017

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A key enzyme of the shikimate pathway, 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS; EC 2.5.1.19), is the known target of the widely used herbicide glyphosate. Glyphosate resistance in Amaranthus palmeri, one of the most troublesome weeds in agriculture, has evolved through increased EPSPS gene copy number. The aim of this work was to study the pleiotropic effects of (i) EPSPS increased transcript abundance due to gene copy number variation (CNV) and of (ii) glyphosate application on the aromatic amino acid (AAA) and branched chain amino acid (BCAA) synthesis pathways. Hydroponically grown glyphosate sensitive (GS) and glyphosate resistant (GR) plants were treated with glyphosate 3 days after treatment. In absence of glyphosate treatment, high EPSPS gene copy number had only a subtle effect on transcriptional regulation of AAA and BCAA pathway genes. In contrast, glyphosate treatment provoked a general accumulation of the transcripts corresponding to genes of the AAA pathway leading to synthesis of chorismate in both GS and GR. After chorismate, anthranilate synthase transcript abundance was higher while chorismate mutase transcription showed a small decrease in GR and remained stable in GS, suggesting a regulatory branch point in the pathway that favors synthesis toward tryptophan over phenylalanine and tyrosine after glyphosate treatment. This was confirmed by studying enzyme activities in vitro and amino acid analysis. Importantly, this upregulation was glyphosate dose dependent and was observed similarly in both GS and GR populations. Glyphosate treatment also had a slight effect on the expression of BCAA genes but no general effect on the pathway could be observed. Taken together, our observations suggest that the high CNV of EPSPS in A. palmeri GR populations has no major pleiotropic effect on the expression of AAA biosynthetic genes, even in response to glyphosate treatment. This finding supports the idea that the fitness cost associated with EPSPS CNV in A. palmeri may be limited.

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Section: Discussionsupporting

confidence: 83%

Section: Methodsmentioning

confidence: 99%

Effects of EPSPS Copy Number Variation (CNV) and Glyphosate Application on the Aromatic and Branched Chain Amino Acid Synthesis Pathways in Amaranthus palmeri

et al. 2017

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“…Although several short-term biochemical studies have been published recently [17][18][19][20], the originality of this study involves the wide time span used, covering a full period from the initial phases (when plants did not look affected) until when they were visually injured. The measurements performed in this work at the different phases of the treatment (days 1 and 3) and the continuation for 15 days allowed evaluation of the pattern of the shikimate pathway from the onset of the treatment until severe injury.…”

Section: Resultsmentioning

confidence: 99%

The pattern of shikimate pathway and phenylpropanoids after inhibition by glyphosate or quinate feeding in pea roots

Zabalza

Orcaray

Fernández-Escalada

et al. 2017

Pesticide Biochemistry and Physiology

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The shikimate pathway is a metabolic route for the biosynthesis of aromatic amino acids (AAAs) (i.e. phenylalanine, tyrosine, and tryptophan). A key enzyme of shikimate pathway (5-enolpyruvylshikimate-3-phosphate synthase, EPSPS) is the target of the widely used herbicide glyphosate. Quinate is a compound synthesized in plants through a side branch of the shikimate pathway. Glyphosate provokes quinate accumulation and exogenous quinate application to plants shows a potential role of quinate in the toxicity of the herbicide glyphosate. Based on this, we hypothesized that the role of quinate accumulation in the toxicity of the glyphosate would be mediated by a deregulation of the shikimate pathway. In this study the effect of the glyphosate and of the exogenous quinate was evaluated in roots of pea plants by analyzing the time course of a full metabolic map of several metabolites of shikimate and phenylpropanoid pathways. Glyphosate application induced an increase of the 3-deoxy-D-arabino-heptulosonate-7-phosphate synthase (DAHPS, first enzyme of the shikimate pathway) protein and accumulation of metabolites upstream of the enzyme EPSPS. No common effects on the metabolites and regulation of shikimate pathway were detected between quinate and glyphosate treatments, supporting that the importance of quinate in the mode of action of glyphosate is not mediated by a common alteration of the regulation of the shikimate pathway. Contrary to glyphosate, the exogenous quinate supplied was probably incorporated into the main trunk from the branch pathway and accumulated in the final products, such as lignin, concomitant with a decrease in the amount of DAHPS protein.

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“…Previous findings showed that both AHAS and EPSPS inhibitors cause growth arrest followed by a slow plant death of the herbicide-treated plants although they act upon different pathways [5,6]. Both types of herbicides provoke an accumulation of free amino acids [3,[7][8][9][10][11]. This effect is accompanied by a decrease in the soluble protein content [9,11,12] and may be the key to the common response that has been associated with a plant proteolysis response [9].…”

Section: Introductionmentioning

confidence: 99%

Induction of the PDH bypass and upregulation of the ALDH7B4 in plants treated with herbicides inhibiting amino acid biosynthesis

et al. 2017

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Imazamox and glyphosate represent two classes of herbicides that inhibit the activity of acetohydroxyacid synthase in the branched-chain amino acid biosynthesis pathway and the activity of 5-enolpyruvylshikimate-3-phosphate synthase in the aromatic amino acid biosynthesis pathway, respectively. However, it is still unclear how imazamox and glyphosate lead to plant death. Both herbicides inhibit amino-acid biosynthesis and were found to induce ethanol fermentation in plants, but an Arabidopsis mutant deficient in alcohol dehydrogenase 1 was neither more susceptible nor more resistant than the wild-type to the herbicides. In this study, we investigated the effects of the amino acid biosynthesis inhibitors, imazamox and glyphosate, on the pyruvate dehydrogenase bypass reaction and fatty acid metabolism in A. thaliana. We found that the pyruvate dehydrogenase bypass was upregulated following the treatment by the two herbicides. Our results suggest that the Arabidopsis aldehyde dehydrogenase 7B4 gene might be participating in the pyruvate dehydrogenase bypass reaction. We evaluated the potential role of the aldehyde dehydrogenase 7B4 upon herbicide treatment in the plant defence mechanism. Plants that overexpressed the ALDH7B4 gene accumulated less soluble sugars, starch, and fatty acids and grew better than the wild-type after herbicide treatment. We discuss how the upregulation of the ALDH7B4 alleviates the effects of the herbicides, potentially through the detoxification of the metabolites produced in the pyruvate dehydrogenase bypass.

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Metabolic Profiling and Enzyme Analyses Indicate a Potential Role of Antioxidant Systems in Complementing Glyphosate Resistance in an Amaranthus palmeri Biotype

Cited by 65 publications

References 53 publications

Effects of EPSPS Copy Number Variation (CNV) and Glyphosate Application on the Aromatic and Branched Chain Amino Acid Synthesis Pathways in Amaranthus palmeri

Effects of EPSPS Copy Number Variation (CNV) and Glyphosate Application on the Aromatic and Branched Chain Amino Acid Synthesis Pathways in Amaranthus palmeri

The pattern of shikimate pathway and phenylpropanoids after inhibition by glyphosate or quinate feeding in pea roots

Induction of the PDH bypass and upregulation of the ALDH7B4 in plants treated with herbicides inhibiting amino acid biosynthesis

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