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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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Changes in phytohormone concentrations in cotton, corn, and tomato plants treated with the neonicotinoid insecticides.Applications of thiamethoxam to cotton plants (N = 8) significantly decreased levels of OPDA (A). Concentrations of this phytohormone were seven times lower in these plants than in untreated cotton. Similar effect on this phytohormone was noted in corn plants (N = 8) exposed to clothianidin, where OPDA was reduced by 50% compared to untreated corn (B). Imidacloprid applied to tomato plants (N = 8) also lowered quantities of OPDA (C). While the OPDA concentrations were reduced significantly in these plants, levels of total SA increased over three times in tomato plants treated with imidacloprid (D). Four-week old plants were used in the experiment. Tomato plants were treated with soil applications of imidacloprid seven days prior to the experiment. Values are means±one standard error. Asterisks mark means that are significantly different (P<0.05; ANOVA, mixed model or Kruskal-Wallis test).
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pone-0062620-g003: Changes in phytohormone concentrations in cotton, corn, and tomato plants treated with the neonicotinoid insecticides.Applications of thiamethoxam to cotton plants (N = 8) significantly decreased levels of OPDA (A). Concentrations of this phytohormone were seven times lower in these plants than in untreated cotton. Similar effect on this phytohormone was noted in corn plants (N = 8) exposed to clothianidin, where OPDA was reduced by 50% compared to untreated corn (B). Imidacloprid applied to tomato plants (N = 8) also lowered quantities of OPDA (C). While the OPDA concentrations were reduced significantly in these plants, levels of total SA increased over three times in tomato plants treated with imidacloprid (D). Four-week old plants were used in the experiment. Tomato plants were treated with soil applications of imidacloprid seven days prior to the experiment. Values are means±one standard error. Asterisks mark means that are significantly different (P<0.05; ANOVA, mixed model or Kruskal-Wallis test).

Mentions: Concentrations of OPDA were consistently reduced by applications of thiamethoxam, clothianidin, and imidacloprid (Fig. 3). Thiamethoxam applications to cotton had the greatest effect on this phytohormone; OPDA levels in thiamethoxam-treated cotton were nearly 15 times lower than in untreated cotton (X2 = 10.42, df = 1, P = 0.001; Fig. 3A). Clothianidin applications to corn decreased concentrations of OPDA by 50% (F1,14 = 6.12, P = 0.03; Fig. 3B), and levels of OPDA in imidacloprid-treated tomato were 3.5 times lower than in untreated tomato plants (X2 = 10.39, df = 1, P = 0.001; Fig. 3C). The effect of the neonicotinoid insecticide imidacloprid on tomato, however, was strikingly different. Imidacloprid applications significantly increased quantities of SA (F1,14 = 21.89, P<0.001; Fig. 3D). Total SA concentrations were three times higher in treated plants. It is also noteworthy that imidacloprid and clothianidin marginally affected several other phytohormones in tomato and corn, respectively. Imidacloprid lowered levels of JA and JA-Ile in tomato plants, and clothianidin decreased concentrations of ABA and JA in corn plants (Table 1).


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)

Changes in phytohormone concentrations in cotton, corn, and tomato plants treated with the neonicotinoid insecticides.Applications of thiamethoxam to cotton plants (N = 8) significantly decreased levels of OPDA (A). Concentrations of this phytohormone were seven times lower in these plants than in untreated cotton. Similar effect on this phytohormone was noted in corn plants (N = 8) exposed to clothianidin, where OPDA was reduced by 50% compared to untreated corn (B). Imidacloprid applied to tomato plants (N = 8) also lowered quantities of OPDA (C). While the OPDA concentrations were reduced significantly in these plants, levels of total SA increased over three times in tomato plants treated with imidacloprid (D). Four-week old plants were used in the experiment. Tomato plants were treated with soil applications of imidacloprid seven days prior to the experiment. Values are means±one standard error. Asterisks mark means that are significantly different (P<0.05; ANOVA, mixed model or Kruskal-Wallis test).
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3643937&req=5

pone-0062620-g003: Changes in phytohormone concentrations in cotton, corn, and tomato plants treated with the neonicotinoid insecticides.Applications of thiamethoxam to cotton plants (N = 8) significantly decreased levels of OPDA (A). Concentrations of this phytohormone were seven times lower in these plants than in untreated cotton. Similar effect on this phytohormone was noted in corn plants (N = 8) exposed to clothianidin, where OPDA was reduced by 50% compared to untreated corn (B). Imidacloprid applied to tomato plants (N = 8) also lowered quantities of OPDA (C). While the OPDA concentrations were reduced significantly in these plants, levels of total SA increased over three times in tomato plants treated with imidacloprid (D). Four-week old plants were used in the experiment. Tomato plants were treated with soil applications of imidacloprid seven days prior to the experiment. Values are means±one standard error. Asterisks mark means that are significantly different (P<0.05; ANOVA, mixed model or Kruskal-Wallis test).
Mentions: Concentrations of OPDA were consistently reduced by applications of thiamethoxam, clothianidin, and imidacloprid (Fig. 3). Thiamethoxam applications to cotton had the greatest effect on this phytohormone; OPDA levels in thiamethoxam-treated cotton were nearly 15 times lower than in untreated cotton (X2 = 10.42, df = 1, P = 0.001; Fig. 3A). Clothianidin applications to corn decreased concentrations of OPDA by 50% (F1,14 = 6.12, P = 0.03; Fig. 3B), and levels of OPDA in imidacloprid-treated tomato were 3.5 times lower than in untreated tomato plants (X2 = 10.39, df = 1, P = 0.001; Fig. 3C). The effect of the neonicotinoid insecticide imidacloprid on tomato, however, was strikingly different. Imidacloprid applications significantly increased quantities of SA (F1,14 = 21.89, P<0.001; Fig. 3D). Total SA concentrations were three times higher in treated plants. It is also noteworthy that imidacloprid and clothianidin marginally affected several other phytohormones in tomato and corn, respectively. Imidacloprid lowered levels of JA and JA-Ile in tomato plants, and clothianidin decreased concentrations of ABA and JA in corn plants (Table 1).

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