Abstract

The tarnished plant bug has become increasingly resistant to organophosphates in recent years. To better understand acephate resistance mechanisms, biological, biochemical, and molecular experiments were systematically conducted with susceptible (LLS) and acephate-selected (LLR) strains. Selection of a field population with acephate significantly increased resistance ratio to 5.9-fold, coupled with a significant increase of esterase activities by 2-fold. Microarray analysis of 6,688 genes revealed 329 up- and 333 down-regulated (≥2-fold) genes in LLR. Six esterase, three P450, and one glutathione S-transferase genes were significantly up-regulated, and no such genes were down-regulated in LLR. All vitellogenin and eggshell protein genes were significantly down-regulated in LLR. Thirteen protease genes were significantly down-regulated and only 3 were up-regulated in LLR. More than twice the number of catalysis genes and more than 3.6-fold of metabolic genes were up-regulated, respectively, as compared to those down-regulated with the same molecular and biological functions. The large portion of metabolic or catalysis genes with significant up-regulations indicated a substantial increase of metabolic detoxification in LLR. Significant increase of acephate resistance, increases of esterase activities and gene expressions, and variable esterase sequences between LLS and LLR consistently demonstrated a major esterase-mediated resistance in LLR, which was functionally provable by abolishing the resistance with esterase inhibitors. In addition, significant elevation of P450 gene expression and reduced susceptibility to imidacloprid in LLR indicated a concurrent resistance risk that may impact other classes of insecticides. This study demonstrated the first association of down-regulation of reproductive- and digestive-related genes with resistance to conventional insecticides, suggesting potential fitness costs associated with resistance development. This study shed new light on the understanding of the molecular basis of insecticide resistance, and the information is highly valuable for development of chemical control guidelines and tactics to minimize resistance and cross-resistance risks.

Highlights

  • During the last decade, widespread adoptions of transgenic Bt cotton and altered chemical control schemes have allowed sucking insect populations to increase

  • Esterase activity determined with a-NA was 2.5-fold higher in laboratory susceptible strain (LLS). A field population (Lula) field population and 4.5-fold higher in the acephate selected bugs (Lula600) than LLS

  • We consistently demonstrated that esterases are major detoxification enzymes and are responsible for the metabolic resistance closely associated with increased acephate resistance in the tarnished plant bug

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Summary

Introduction

Widespread adoptions of transgenic Bt cotton and altered chemical control schemes have allowed sucking insect populations to increase. Of these pests, the tarnished plant bug (TPB), Lygus lineolaris, emerged as the most economically significant [1]. Management of tarnished plant bug relies almost exclusively on chemical control. An organophosphorus insecticide, is among the most widely used insecticides for TPB control. In order to suppress feeding damages from tarnished plant bug and bollworm/tobacco budworm, cotton is more frequently sprayed than other major crops in the South. Over the years, tarnished plant bug has become increasingly resistant to several chemical insecticides [2,3,4], including acephate [5]

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