Anthropogenic effects on plant resistance: Can insecticides alter induction of defenses in crop plants?

Background/Question/Methods

The vast majority of agroecosystems are constantly exposed to a myriad of chemicals applied to suppress economically important arthropods. Many of the new insecticides are formulated to lessen their impact on non-target organisms by confining the chemicals to plant tissues. Neonicotinoid insecticides are one of the most frequently used systemic insecticides, and have remarkably long residual toxicity and broad-spectrum activity. Neonicotinoids, however, have been associated with severe outbreaks of non-susceptible herbivores, spider mites. Moreover, it was recently discovered that these insecticides interact directly with plant resistance by inducing defense pathways regulated by a phytohormone salicylic acid. Our goal was to examine if several neonicotinoids disrupt natural plant defenses, and if direct effects on induction of defenses is correlated with increases in populations of spider mites on diverse crop plants. Therefore, we quantified expression of several genes involved in induced defenses in tomato, cotton and corn plants exposed to three neonicotinoids, imidacloprid, thiamethoxam and clothianidin. We also measured concentrations of phytohormones, and we evaluated spider mite performance on these diverse crop plants. 

Results/Conclusions

We found that expression of defense genes and concentrations of phytohormones in plants exposed to the neonicotinoid insecticides were significantly different from untreated plants. In particular, neonicotinoid insecticides suppressed expression of phenylalanine amonia lyase, coenzyme A ligase, trypsin protease inhibitor and chitinase. 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. Our findings illustrate that insecticide-driven disruption of plant defenses can result in elevated populations of unsusceptible herbivores. This study adds to growing evidence that agrochemicals can have unanticipated ecological effects and suggests that the direct effects of insecticides on plant defenses should be considered when non-target impacts of insecticides are evaluated.