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

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 vo...

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Veröffentlicht in:Molecular ecology 2013-11, Vol.22 (22), p.5624-5634
Hauptverfasser: Ge, Lin-Quan, Huang, Liu-Juan, Yang, Guo-Qin, Song, Qi-Sheng, Stanley, David, Gurr, G. M., Wu, Jin-Cai
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container_issue 22
container_start_page 5624
container_title Molecular ecology
container_volume 22
creator Ge, Lin-Quan
Huang, Liu-Juan
Yang, Guo-Qin
Song, Qi-Sheng
Stanley, David
Gurr, G. M.
Wu, Jin-Cai
description 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 sub
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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. 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Biological and molecular evolution ; heat-shock proteins ; Hemiptera ; Hemiptera - drug effects ; Hemiptera - genetics ; Hemiptera - physiology ; HSP72 Heat-Shock Proteins - genetics ; Insect Proteins - genetics ; insecticides ; Insecticides - pharmacology ; Nilaparvata lugens ; Nymph - drug effects ; Nymph - physiology ; Organothiophosphates - pharmacology ; Oryza sativa ; Population genetics, reproduction patterns ; RNA Interference ; Stress, Physiological ; Temperature ; thermotolerance ; Triazoles - pharmacology</subject><ispartof>Molecular ecology, 2013-11, Vol.22 (22), p.5624-5634</ispartof><rights>2013 John Wiley &amp; Sons Ltd</rights><rights>2015 INIST-CNRS</rights><rights>2013 John Wiley &amp; Sons Ltd.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fmec.12502$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fmec.12502$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&amp;idt=27999195$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24303791$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ge, Lin-Quan</creatorcontrib><creatorcontrib>Huang, Liu-Juan</creatorcontrib><creatorcontrib>Yang, Guo-Qin</creatorcontrib><creatorcontrib>Song, Qi-Sheng</creatorcontrib><creatorcontrib>Stanley, David</creatorcontrib><creatorcontrib>Gurr, G. M.</creatorcontrib><creatorcontrib>Wu, Jin-Cai</creatorcontrib><title>Molecular basis for insecticide-enhanced thermotolerance in the brown planthopper Nilaparvata lugens Stål (Hemiptera:Delphacidae)</title><title>Molecular ecology</title><addtitle>Mol Ecol</addtitle><description>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. 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Biological and molecular evolution</subject><subject>heat-shock proteins</subject><subject>Hemiptera</subject><subject>Hemiptera - drug effects</subject><subject>Hemiptera - genetics</subject><subject>Hemiptera - physiology</subject><subject>HSP72 Heat-Shock Proteins - genetics</subject><subject>Insect Proteins - genetics</subject><subject>insecticides</subject><subject>Insecticides - pharmacology</subject><subject>Nilaparvata lugens</subject><subject>Nymph - drug effects</subject><subject>Nymph - physiology</subject><subject>Organothiophosphates - pharmacology</subject><subject>Oryza sativa</subject><subject>Population genetics, reproduction patterns</subject><subject>RNA Interference</subject><subject>Stress, Physiological</subject><subject>Temperature</subject><subject>thermotolerance</subject><subject>Triazoles - pharmacology</subject><issn>0962-1083</issn><issn>1365-294X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkVtvFCEYhomxsdvqhX_AcGPSXkwLDIfBO7O2XXVbYzzeEYYBF2UOwkwPt_6X_hL_mGx3rZeSEMjH8358eV8AnmJ0hPM6bq05woQh8gDMcMlZQST9-hDMkOSkwKgqd8FeSt8RwiVh7BHYJbREpZB4Bn6d98GaKegIa518gq6P0HfJmtEb39jCdivdGdvAcWVj248Zj-tChtYlWMf-qoND0N246ofBRnjhgx50vNSjhmH6ZrsEP4y_bwM8WNjWD2PWv3hlw7DS-QNtDx-DHadDsk-25z74dHrycb4olu_OXs9fLgtPuCCF1LxuGlEb4xjmTvDGcSYIxVpUHBuBnMOMGZQNQbTikjBKMMGu4g4LQ0W5Dw42fYfY_5xsGlXrk7Ehj277KSnMEM2bU_l_lHKah6hKktFnW3SqW9uoIfpWxxv11-IMPN8COhkd3No9n_5xQkqJJcvc8Ya78sHe3L9jpNYZq5yxustYnZ_M7y5ZUWwUPo32-l6h4w_FRSmY-nJxphanb97OP79naln-AbNBqLo</recordid><startdate>201311</startdate><enddate>201311</enddate><creator>Ge, Lin-Quan</creator><creator>Huang, Liu-Juan</creator><creator>Yang, Guo-Qin</creator><creator>Song, Qi-Sheng</creator><creator>Stanley, David</creator><creator>Gurr, G. M.</creator><creator>Wu, Jin-Cai</creator><general>Blackwell Publishing Ltd</general><general>Blackwell</general><scope>BSCLL</scope><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7TV</scope><scope>7U6</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>201311</creationdate><title>Molecular basis for insecticide-enhanced thermotolerance in the brown planthopper Nilaparvata lugens Stål (Hemiptera:Delphacidae)</title><author>Ge, Lin-Quan ; Huang, Liu-Juan ; Yang, Guo-Qin ; Song, Qi-Sheng ; Stanley, David ; Gurr, G. 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M.</au><au>Wu, Jin-Cai</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Molecular basis for insecticide-enhanced thermotolerance in the brown planthopper Nilaparvata lugens Stål (Hemiptera:Delphacidae)</atitle><jtitle>Molecular ecology</jtitle><addtitle>Mol Ecol</addtitle><date>2013-11</date><risdate>2013</risdate><volume>22</volume><issue>22</issue><spage>5624</spage><epage>5634</epage><pages>5624-5634</pages><issn>0962-1083</issn><eissn>1365-294X</eissn><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.</abstract><cop>Oxford</cop><pub>Blackwell Publishing Ltd</pub><pmid>24303791</pmid><doi>10.1111/mec.12502</doi><tpages>11</tpages></addata></record>
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subjects Animals
arginine kinase
Arginine Kinase - genetics
Biological and medical sciences
Biological evolution
brown planthopper
Climate Change
Delphacidae
Female
Fundamental and applied biological sciences. Psychology
Genetics of eukaryotes. Biological and molecular evolution
heat-shock proteins
Hemiptera
Hemiptera - drug effects
Hemiptera - genetics
Hemiptera - physiology
HSP72 Heat-Shock Proteins - genetics
Insect Proteins - genetics
insecticides
Insecticides - pharmacology
Nilaparvata lugens
Nymph - drug effects
Nymph - physiology
Organothiophosphates - pharmacology
Oryza sativa
Population genetics, reproduction patterns
RNA Interference
Stress, Physiological
Temperature
thermotolerance
Triazoles - pharmacology
title Molecular basis for insecticide-enhanced thermotolerance in the brown planthopper Nilaparvata lugens Stål (Hemiptera:Delphacidae)
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