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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 spider mite herbivory on expression 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). Spider mites induced expression of CoA ligase and chitinase in cotton (A), and elicited significant expression of all four genes in corn (B). Trypsin PI was the only defense gene induced by spider mites in tomato (C).
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pone-0062620-g001: Effect of spider mite herbivory on expression 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). Spider mites induced expression of CoA ligase and chitinase in cotton (A), and elicited significant expression of all four genes in corn (B). Trypsin PI was the only defense gene induced by spider mites in tomato (C).

Mentions: In cotton plants, spider mite feeding induced a 11-fold increase in expression of CoA ligase and a seven-fold increase in expression of chitinase (Fig. 1A). Expression of trypsin PI was slightly elevated in infested cotton plants, but did not differ significantly from plants free of the herbivore. In untreated corn, spider mite feeding significantly increased the expression of all four genes. Transcripts of PAL increased 4.5 fold, CoA ligase 11.2 fold, trypsin PI 1.49 fold, and chitinase 3.2 fold compared to uninfested corn (Fig. 1B). In tomato plants, spider mite feeding induced the expression of trypsin PI by 1.8 fold, while expression of the remaining genes was not significantly affected by spider mite herbivory (Fig. 1C).


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 spider mite herbivory on expression 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). Spider mites induced expression of CoA ligase and chitinase in cotton (A), and elicited significant expression of all four genes in corn (B). Trypsin PI was the only defense gene induced by spider mites in tomato (C).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3643937&req=5

pone-0062620-g001: Effect of spider mite herbivory on expression 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). Spider mites induced expression of CoA ligase and chitinase in cotton (A), and elicited significant expression of all four genes in corn (B). Trypsin PI was the only defense gene induced by spider mites in tomato (C).
Mentions: In cotton plants, spider mite feeding induced a 11-fold increase in expression of CoA ligase and a seven-fold increase in expression of chitinase (Fig. 1A). Expression of trypsin PI was slightly elevated in infested cotton plants, but did not differ significantly from plants free of the herbivore. In untreated corn, spider mite feeding significantly increased the expression of all four genes. Transcripts of PAL increased 4.5 fold, CoA ligase 11.2 fold, trypsin PI 1.49 fold, and chitinase 3.2 fold compared to uninfested corn (Fig. 1B). In tomato plants, spider mite feeding induced the expression of trypsin PI by 1.8 fold, while expression of the remaining genes was not significantly affected by spider mite herbivory (Fig. 1C).

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