Classification of the glyphosate target enzyme (5-enolpyruvylshikimate-3-phosphate synthase) for assessing sensitivity of organisms to the herbicide

Leino, Lyydia; Tall, Tuomas; Helander, Marjo; Saloniemi, Irma; Saikkonen, Kari; Ruuskanen, Suvi; Puigbò, Pere

doi:10.1016/j.jhazmat.2020.124556

Cited by 73 publications

(102 citation statements)

References 42 publications

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“…We analysed 663 microbial genomes distributed across 32 alignable tight genomic clusters (ATGCs) (Novichkov et al ., 2009; Puigbò et al ., 2014), with the EPSPSClass server (http://ppuigbo.me/programs/EPSPSClass) (Leino et al ., 2020) to identify changes in sensitivity to glyphosate. The algorithm classifies EPSPS proteins based on the presence and absence of amino acid markers in the active site that determine whether the enzyme is putatively sensitive (class I) or resistant (class II, III and IV) to the glyphosate (see methods).…”

Section: Resultsmentioning

confidence: 99%

“…Glyphosate inhibits the shikimate pathway by inhibiting the enzyme EPSPS (Schönbrunn et al, 2001;Abraham, 2020). The EPSPS class has been classified with the EPSPSClass server (http://ppuigbo.me/programs/ EPSPSClass), which assesses the type of potential sensitivity of the EPSPS enzyme to the herbicide glyphosate (Leino et al, 2020). The amino acid markers to determine potential glyphosate sensitivity to glyphosate (Supplementary Table 10) are also available at Leino et al (2020)) and in the web server.…”

Section: Classification Of the Epspsmentioning

confidence: 99%

“…The EPSPS class has been classified with the EPSPSClass server (http://ppuigbo.me/programs/ EPSPSClass), which assesses the type of potential sensitivity of the EPSPS enzyme to the herbicide glyphosate (Leino et al, 2020). The amino acid markers to determine potential glyphosate sensitivity to glyphosate (Supplementary Table 10) are also available at Leino et al (2020)) and in the web server. EPSPS enzymes can be classified as class I (alpha or beta) (Light et al, 2016;Firdous et al, 2018), class II (Barry et al, 1997;Priestman et al, 2005), III (Carozzi et al, 2006) or IV (Lira et al, 2013) based on the presence of known amino acid markers (class I, class II and class IV) and motifs (class III) (Barry et al, 1997;Priestman et al, 2005;Carozzi et al, 2006;Lira et al, 2013;Light et al, 2016;Firdous et al, 2018).…”

Section: Classification Of the Epspsmentioning

confidence: 99%

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Adaptation of bacteria to glyphosate: a microevolutionary perspective of the enzyme 5‐enolpyruvylshikimate‐3‐phosphate synthase

Rainio

Ruuskanen

Helander

et al. 2021

Environ Microbiol Rep

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Glyphosate is the leading herbicide worldwide, but it also affects prokaryotes because it targets the central enzyme (5-enolpyruvylshikimate-3-phosphate, EPSP) of the shikimate pathway in the synthesis of the three essential aromatic amino acids in bacteria, fungi and plants. Our results reveal that bacteria may easily become resistant to glyphosate through changes in the 5-enolpyruvylshikimate-3-phosphate synthase active site. This indicates the importance of examining how glyphosate affects microbe-mediated ecosystem functions and human microbiomes.

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Section: Resultsmentioning

confidence: 99%

Section: Classification Of the Epspsmentioning

confidence: 99%

Section: Classification Of the Epspsmentioning

confidence: 99%

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Adaptation of bacteria to glyphosate: a microevolutionary perspective of the enzyme 5‐enolpyruvylshikimate‐3‐phosphate synthase

Rainio

Ruuskanen

Helander

et al. 2021

Environ Microbiol Rep

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“…Glyphosate may be able to interact in two ways with plant-associated microbes: (i) by directly affecting their metabolism, especially those sharing the shikimate pathway, such as several fungal and bacterial guilds [80,81]; or (ii) indirectly, by inducing a substantial change in the plant metabolome, which is essential to the status of plant-fungi symbioses [40,82] (Figure 2). Signaling between plants and associated microbes can depend on plant metabolites derived from the shikimate pathway, such as flavonoids, which are essential for successful nodulation between legumes and nitrogen-fixing rhizobacteria [83].…”

Section: Box 2 Indirect Effects Of Glyphosate On Plant-associated Microbesmentioning

confidence: 99%

Glyphosate-Modulated Biosynthesis Driving Plant Defense and Species Interactions

Fuchs

Saikkonen

Helander

2021

Trends in Plant Science

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Glyphosate has become the best-selling herbicide used in agriculture, horticulture, silviculture, and urban environments. It disrupts the shikimate metabolic pathway and thereby blocks the production of aromatic amino acids, which are the basis for several plant metabolites. Glyphosate residues are reported in soils from diverse environments, but the effects on plant physiology and consequences for species interactions are largely unknown. Here, we emphasize the complexity of these physiological processes, and argue that glyphosate residues modulate biosynthetic pathways, individually or interactively, which may affect interactions between plants and heterotrophic organisms. In this way, glyphosate residues can substantially interfere with plant resistance and the attraction of beneficial insects, both of which are essential elements in integrated pest management and healthy ecosystems. Glyphosate Residues Affect Plant Defense Compound Biosynthesis HighlightsResidues of glyphosate, a potent herbicide, are increasingly found in diverse environments.Glyphosate residues in soil alter plant physiological processes; however, their effects on plant defense strategies and subsequent species interactions are poorly understood.Glyphosate inhibition of the shikimate pathway affects plant defense-related phytohormones and the phenylpropanoid pathway, the basis for many phytoalexins.Glyphosate affects lipid peroxidation, which alters jasmonic acid levels and green leaf volatiles, in turn, important players mediating many trophic interactions and pollinator attraction.By changing the plant biochemistry, glyphosate residues in soil have the potential to alter plant interactions with herbivores and mutualistic organisms.

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“…While these compounds are thought to be specific to plants, they can cause collateral damage to other types of organisms by targeting evolutionarily conserved pathways ( Motta et al. 2018 ; Leino et al. 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Herbicide Selection Promotes Antibiotic Resistance in Soil Microbiomes

Liao

Yang

et al. 2021

Molecular Biology and Evolution

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Herbicides are one of the most widely used chemicals in agriculture. While they are known to be harmful to non-target organisms, the effects of herbicides on the composition and functioning of soil microbial communities remain unclear. Here we show that application of three widely used herbicides—glyphosate, glufosinate and dicamba—increase the prevalence of antibiotic resistance genes (ARGs) and mobile genetic elements (MGEs) in soil microbiomes without clear changes in the abundance, diversity and composition of bacterial communities. Mechanistically, these results could be explained by a positive selection for more tolerant genotypes that acquired several mutations in previously well-characterized herbicide and antibiotic resistance genes. Moreover, herbicide exposure increased cell membrane permeability and conjugation frequency of multidrug resistance plasmids, promoting ARG movement between bacteria. A similar pattern was found in agricultural soils across eleven provinces in China, where herbicide application, and the levels of glyphosate residues in soils, were associated with increased ARG and MGE abundances relative to herbicide-free control sites. Together, our results show that herbicide application can enrich ARGs and MGEs by changing the genetic composition of soil microbiomes, potentially contributing to the global antimicrobial resistance problem in agricultural environments.

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Classification of the glyphosate target enzyme (5-enolpyruvylshikimate-3-phosphate synthase) for assessing sensitivity of organisms to the herbicide

Cited by 73 publications

References 42 publications

Adaptation of bacteria to glyphosate: a microevolutionary perspective of the enzyme 5‐enolpyruvylshikimate‐3‐phosphate synthase

Adaptation of bacteria to glyphosate: a microevolutionary perspective of the enzyme 5‐enolpyruvylshikimate‐3‐phosphate synthase

Glyphosate-Modulated Biosynthesis Driving Plant Defense and Species Interactions

Herbicide Selection Promotes Antibiotic Resistance in Soil Microbiomes

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