Molecular basis for insecticide‐enhanced thermotolerance in the brown planthopper Nilaparvata lugens Stål (Hemiptera:Delphacidae)

Abstract

Climate change is likely to have marked ecological effects on terrestrial ecosystems, including the activities of insect pests. Most attention has focused on the increasing geographical ranges of pests; however, if extrinsic factors enhance their thermotolerance, populations may express increased voltinism and longer daily and annual activity periods. These changes in pest populations have the potential for severe consequences, including increased crop losses and decreased food security at the global level. The brown planthopper (BPH) Nilaparvata lugens Stål (Hemiptera: Delphacidae) is a serious pest of rice crops in temperate and tropical regions of Asia. It is often present in rice microclimates at temperatures close to its maximum thermotolerance. Recent BPH outbreaks in tropical Asia are considered to be associated with excess use of pesticides and increasing temperature. This study tested whether exposure to sublethal concentrations of triazophos (tzp), an insecticide widely used in Asian rice production, enhances thermotolerance of BPH. Tzp exposure (40 ppm at 40 °C) significantly decreased mortality (from 94% in controls to 50% at 48 h post-treatment) and increased lethal mean time (LT50 ) of adults by 17.2 h. To investigate the underlying molecular mechanism of this tzp-enhanced thermotolerance, we selected Hsp70 and Arginine kinase (Argk) for detailed study. Transcripts encoding both proteins in third-instar nymphs and brachypterous adult females were up-regulated, compared with controls, after exposure to tzp. RNAi silencing of both genes demonstrated that Hsp70 and Argk are essential for survival and tzp-increased thermotolerance. We propose that tzp induces thermotolerance in BPHs by increasing the expression of genes that act in cell protection mechanisms. The significance of our proposal relates to the importance of understanding the influence of sublethal concentrations of insecticides on pest biology. In addition to its influence on thermotolerance, tzp also enhances BPH reproduction. We infer that exposure to a pesticide stressor can produce cross-tolerance, that is, increased tolerance to one stressor also increases tolerance to other stressors, including temperature. Aside from needing a better understanding of these effects in nature and in other pest/cropping systems, we suggest that pest management programmes can be improved with better understanding of the influences of stressors, including increased environmental temperatures and sublethal concentrations of insecticides, on pest biology.

Driving Pest Insect Populations: Agricultural Chemicals Lead to an Adaptive Syndrome in Nilaparvata Lugens Stål (Hemiptera: Delphacidae)

“…The adaptive syndrome we propose is multi-faceted, including highly increased insecticide resistance2627, increased flight capacity28, increased reproduction and population sizes and, as shown here, enhanced thermolerance15. The increased thermotolerance is noteworthy in light of the biology of BPH, which undergoes weather-dependent, windborne migrations.…”

“…Our demonstration that JGM acts via increasing Hsp70 expression unveils a molecular mechanism of the JGM effects. We note that tzp treatments also led to increased thermotolerance; it is not surprising to see that both tzp and JGM operate via the same gene, Hsp70 15.…”

“…Previous studies demonstrated that Hsp70 contributes to tzp-induced BPH thermotolerance15 and that Acc contributes to JGM-enhanced reproduction20. We selected these two genes for functional analysis of JGM-induced increases in thermotolerance and reproduction.…”

“…BPH outbreaks are associated with temperature, a key parameter for forecasting population outbreaks14. Taken with global warming and with the understanding that some insecticides lead to enhanced thermotolerance and reproduction in BPH15, we are investigating the molecular adaptations to some agricultural chemicals that may lead to catastrophic losses in Asian rice production. Two insecticides, deltamethrin and trizaophos (tzp), stimulate increased BPH reproduction, in part by increasing expression of a gene encoding vitellogenin (Vg)16.…”

“…Consistent with these results, tzp treatments led to increased expression of Hsp70 and Argk . It can be inferred that tzp induces thermotolerance by increasing expression of genes acting in cell protection mechanisms15.…”