Microarray analysis of gene regulations and potential association with acephate-resistance and fitness cost in Lygus lineolaris.

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 o...

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Main Authors: Yu Cheng Zhu, Zibiao Guo, Yueping He, Randall Luttrell
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3360042?pdf=render
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spelling doaj-ef3cdec8e248474ebb6b4f3bce2a1aa02020-11-25T01:44:56ZengPublic Library of Science (PLoS)PLoS ONE1932-62032012-01-0175e3758610.1371/journal.pone.0037586Microarray analysis of gene regulations and potential association with acephate-resistance and fitness cost in Lygus lineolaris.Yu Cheng ZhuZibiao GuoYueping HeRandall LuttrellThe 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.http://europepmc.org/articles/PMC3360042?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Yu Cheng Zhu
Zibiao Guo
Yueping He
Randall Luttrell
spellingShingle Yu Cheng Zhu
Zibiao Guo
Yueping He
Randall Luttrell
Microarray analysis of gene regulations and potential association with acephate-resistance and fitness cost in Lygus lineolaris.
PLoS ONE
author_facet Yu Cheng Zhu
Zibiao Guo
Yueping He
Randall Luttrell
author_sort Yu Cheng Zhu
title Microarray analysis of gene regulations and potential association with acephate-resistance and fitness cost in Lygus lineolaris.
title_short Microarray analysis of gene regulations and potential association with acephate-resistance and fitness cost in Lygus lineolaris.
title_full Microarray analysis of gene regulations and potential association with acephate-resistance and fitness cost in Lygus lineolaris.
title_fullStr Microarray analysis of gene regulations and potential association with acephate-resistance and fitness cost in Lygus lineolaris.
title_full_unstemmed Microarray analysis of gene regulations and potential association with acephate-resistance and fitness cost in Lygus lineolaris.
title_sort microarray analysis of gene regulations and potential association with acephate-resistance and fitness cost in lygus lineolaris.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2012-01-01
description 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.
url http://europepmc.org/articles/PMC3360042?pdf=render
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