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Neonicotinoid insecticides alter induced defenses and increase susceptibility to spider mites in distantly related crop plants.

Szczepaniec A, Raupp MJ, Parker RD, Kerns D, Eubanks MD - PLoS ONE (2013)

Bottom Line: Little research, however, has focused on the direct effects of insecticides on plants.Our findings are important because applications of neonicotinoid insecticides have been associated with outbreaks of spider mites in several unrelated plant species.This study adds to growing evidence that bioactive agrochemicals can have unanticipated ecological effects and suggests that the direct effects of insecticides on plant defenses should be considered when the ecological costs of insecticides are evaluated.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, Texas A&M University, College Station, Texas, United States of America. adrianna.szczepaniec@sdstate.edu

ABSTRACT

Background: Chemical suppression of arthropod herbivores is the most common approach to plant protection. Insecticides, however, can cause unintended, adverse consequences for non-target organisms. Previous studies focused on the effects of pesticides on target and non-target pests, predatory arthropods, and concomitant ecological disruptions. Little research, however, has focused on the direct effects of insecticides on plants. Here we demonstrate that applications of neonicotinoid insecticides, one of the most important insecticide classes worldwide, suppress expression of important plant defense genes, alter levels of phytohormones involved in plant defense, and decrease plant resistance to unsusceptible herbivores, spider mites Tetranychus urticae (Acari: Tetranychidae), in multiple, distantly related crop plants.

Methodology/principal findings: Using cotton (Gossypium hirsutum), corn (Zea mays) and tomato (Solanum lycopersicum) plants, we show that transcription of phenylalanine ammonia lyase, coenzyme A ligase, trypsin protease inhibitor and chitinase are suppressed and concentrations of the phytohormone OPDA and salicylic acid were altered by neonicotinoid insecticides. Consequently, the population growth of spider mites increased from 30% to over 100% on neonicotinoid-treated plants in the greenhouse and by nearly 200% in the field experiment.

Conclusions/significance: Our findings are important because applications of neonicotinoid insecticides have been associated with outbreaks of spider mites in several unrelated plant species. More importantly, this is the first study to document insecticide-mediated disruption of plant defenses and link it to increased population growth of a non-target herbivore. This study adds to growing evidence that bioactive agrochemicals can have unanticipated ecological effects and suggests that the direct effects of insecticides on plant defenses should be considered when the ecological costs of insecticides are evaluated.

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Effect of the neonicotinoid insecticides on transcription of defense genes in cotton, corn, and tomato.Fold induction was calculated relative to plants free of spider mites and not treated with the insecticides (Untreated). Ubiquitin gene was used as an internal standard. All treatments were replicated four times for each plant species. Means with different letters were significantly different at P = 0.05 (Wilcoxon test). In all three plants, the neonicotinoid applications altered transcription of the genes regulated by salicylic acid and jasmonic acid. Expression of CoA ligase and chitinase increased in cotton treated with thiamethoxam independently of spider mite herbivory (A). None of the genes were induced in clothianidin-treated corn, and spider mite herbivory did not elicit gene expression in these plants either (B). Expression profile of tomato plants exposed to imidacloprid was dominated by strong chitinase induction, which was independent of the spider mite presence (C). Expression of trypsin PI, a pivotal plant defense employed against the spider mites, was halted in the imidacloprid-treated plants exposed to T. urticae. Similarly, expression of PAL was suppressed in tomato plants treated with imidacloprid and exposed to the herbivore.
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pone-0062620-g002: Effect of the neonicotinoid insecticides on transcription of defense genes in cotton, corn, and tomato.Fold induction was calculated relative to plants free of spider mites and not treated with the insecticides (Untreated). Ubiquitin gene was used as an internal standard. All treatments were replicated four times for each plant species. Means with different letters were significantly different at P = 0.05 (Wilcoxon test). In all three plants, the neonicotinoid applications altered transcription of the genes regulated by salicylic acid and jasmonic acid. Expression of CoA ligase and chitinase increased in cotton treated with thiamethoxam independently of spider mite herbivory (A). None of the genes were induced in clothianidin-treated corn, and spider mite herbivory did not elicit gene expression in these plants either (B). Expression profile of tomato plants exposed to imidacloprid was dominated by strong chitinase induction, which was independent of the spider mite presence (C). Expression of trypsin PI, a pivotal plant defense employed against the spider mites, was halted in the imidacloprid-treated plants exposed to T. urticae. Similarly, expression of PAL was suppressed in tomato plants treated with imidacloprid and exposed to the herbivore.

Mentions: The effects of the neonicotinoids varied among plant species and among the specific neonicotinoid insecticides. Overall, neonicotinoids altered expression of genes regulated by jasmonic acid (JA), salicylic acid (SA), or genes regulated by both JA and SA pathways. Induction of genes regulated by SA was significantly altered by neonicotinoid treatments in cotton plants. Applications of thiamethoxam alone increased expression of CoA ligase 3.5-fold, and expression of this gene was even higher when spider mites were feeding on neonicotinoid-treated plants (Fig. 2A). Chitinase transcripts were also significantly elicited in thiamethoxam-treated cotton, with 2.5-fold induction in spider mites infested and uninfested cotton plants (Fig. 2A). It is noteworthy that induction of both of these genes was weaker than the 11-fold induction of CoA ligase and the seven-fold induction of chitinase in untreated plants exposed to spider mites feeding (Fig. 1A). Exposure of plants to thiamethoxam also appears to drive induction of both genes independently of spider mite herbivory. In addition to its inducible effect on the defense genes, thiamethoxam suppressed expression of PAL in spider mite infested cotton plants (Fig. 2A). Expression of PAL in these plants was lower than 0.5-fold, and spider mite herbivory did not induce levels of PAL in thiamethoxam-treated cotton.


Neonicotinoid insecticides alter induced defenses and increase susceptibility to spider mites in distantly related crop plants.

Szczepaniec A, Raupp MJ, Parker RD, Kerns D, Eubanks MD - PLoS ONE (2013)

Effect of the neonicotinoid insecticides on transcription of defense genes in cotton, corn, and tomato.Fold induction was calculated relative to plants free of spider mites and not treated with the insecticides (Untreated). Ubiquitin gene was used as an internal standard. All treatments were replicated four times for each plant species. Means with different letters were significantly different at P = 0.05 (Wilcoxon test). In all three plants, the neonicotinoid applications altered transcription of the genes regulated by salicylic acid and jasmonic acid. Expression of CoA ligase and chitinase increased in cotton treated with thiamethoxam independently of spider mite herbivory (A). None of the genes were induced in clothianidin-treated corn, and spider mite herbivory did not elicit gene expression in these plants either (B). Expression profile of tomato plants exposed to imidacloprid was dominated by strong chitinase induction, which was independent of the spider mite presence (C). Expression of trypsin PI, a pivotal plant defense employed against the spider mites, was halted in the imidacloprid-treated plants exposed to T. urticae. Similarly, expression of PAL was suppressed in tomato plants treated with imidacloprid and exposed to the herbivore.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3643937&req=5

pone-0062620-g002: Effect of the neonicotinoid insecticides on transcription of defense genes in cotton, corn, and tomato.Fold induction was calculated relative to plants free of spider mites and not treated with the insecticides (Untreated). Ubiquitin gene was used as an internal standard. All treatments were replicated four times for each plant species. Means with different letters were significantly different at P = 0.05 (Wilcoxon test). In all three plants, the neonicotinoid applications altered transcription of the genes regulated by salicylic acid and jasmonic acid. Expression of CoA ligase and chitinase increased in cotton treated with thiamethoxam independently of spider mite herbivory (A). None of the genes were induced in clothianidin-treated corn, and spider mite herbivory did not elicit gene expression in these plants either (B). Expression profile of tomato plants exposed to imidacloprid was dominated by strong chitinase induction, which was independent of the spider mite presence (C). Expression of trypsin PI, a pivotal plant defense employed against the spider mites, was halted in the imidacloprid-treated plants exposed to T. urticae. Similarly, expression of PAL was suppressed in tomato plants treated with imidacloprid and exposed to the herbivore.
Mentions: The effects of the neonicotinoids varied among plant species and among the specific neonicotinoid insecticides. Overall, neonicotinoids altered expression of genes regulated by jasmonic acid (JA), salicylic acid (SA), or genes regulated by both JA and SA pathways. Induction of genes regulated by SA was significantly altered by neonicotinoid treatments in cotton plants. Applications of thiamethoxam alone increased expression of CoA ligase 3.5-fold, and expression of this gene was even higher when spider mites were feeding on neonicotinoid-treated plants (Fig. 2A). Chitinase transcripts were also significantly elicited in thiamethoxam-treated cotton, with 2.5-fold induction in spider mites infested and uninfested cotton plants (Fig. 2A). It is noteworthy that induction of both of these genes was weaker than the 11-fold induction of CoA ligase and the seven-fold induction of chitinase in untreated plants exposed to spider mites feeding (Fig. 1A). Exposure of plants to thiamethoxam also appears to drive induction of both genes independently of spider mite herbivory. In addition to its inducible effect on the defense genes, thiamethoxam suppressed expression of PAL in spider mite infested cotton plants (Fig. 2A). Expression of PAL in these plants was lower than 0.5-fold, and spider mite herbivory did not induce levels of PAL in thiamethoxam-treated cotton.

Bottom Line: Little research, however, has focused on the direct effects of insecticides on plants.Our findings are important because applications of neonicotinoid insecticides have been associated with outbreaks of spider mites in several unrelated plant species.This study adds to growing evidence that bioactive agrochemicals can have unanticipated ecological effects and suggests that the direct effects of insecticides on plant defenses should be considered when the ecological costs of insecticides are evaluated.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, Texas A&M University, College Station, Texas, United States of America. adrianna.szczepaniec@sdstate.edu

ABSTRACT

Background: Chemical suppression of arthropod herbivores is the most common approach to plant protection. Insecticides, however, can cause unintended, adverse consequences for non-target organisms. Previous studies focused on the effects of pesticides on target and non-target pests, predatory arthropods, and concomitant ecological disruptions. Little research, however, has focused on the direct effects of insecticides on plants. Here we demonstrate that applications of neonicotinoid insecticides, one of the most important insecticide classes worldwide, suppress expression of important plant defense genes, alter levels of phytohormones involved in plant defense, and decrease plant resistance to unsusceptible herbivores, spider mites Tetranychus urticae (Acari: Tetranychidae), in multiple, distantly related crop plants.

Methodology/principal findings: Using cotton (Gossypium hirsutum), corn (Zea mays) and tomato (Solanum lycopersicum) plants, we show that transcription of phenylalanine ammonia lyase, coenzyme A ligase, trypsin protease inhibitor and chitinase are suppressed and concentrations of the phytohormone OPDA and salicylic acid were altered by neonicotinoid insecticides. Consequently, the population growth of spider mites increased from 30% to over 100% on neonicotinoid-treated plants in the greenhouse and by nearly 200% in the field experiment.

Conclusions/significance: Our findings are important because applications of neonicotinoid insecticides have been associated with outbreaks of spider mites in several unrelated plant species. More importantly, this is the first study to document insecticide-mediated disruption of plant defenses and link it to increased population growth of a non-target herbivore. This study adds to growing evidence that bioactive agrochemicals can have unanticipated ecological effects and suggests that the direct effects of insecticides on plant defenses should be considered when the ecological costs of insecticides are evaluated.

Show MeSH
Related in: MedlinePlus