The mRNA Expression Profiles of Five Heat Shock Protein Genes from Frankliniella occidentalis at Different Stages and Their Responses to Temperatures and Insecticides

doi:10.1016/S2095-3119(13)60680-2

Journal of Integrative Agriculture ›› 2014, Vol. 13 ›› Issue (10): 2196-2210.DOI: 10.1016/S2095-3119(13)60680-2

The mRNA Expression Profiles of Five Heat Shock Protein Genes from Frankliniella occidentalis at Different Stages and Their Responses to Temperatures and Insecticides

WANG Hai-hong, Stuart R Reitz, WANG Li-xia, WANG Shuai-yu, LI Xue , LEI Zhong-ren

1、State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences,
Beijing 100193, P.R.China
2、Malheur County Extension, Oregon State University, Ontario 97914, USA
3、The General Station of Plant Protection in Shandong, Jinan 250100, P.R.China

收稿日期:2013-07-02 出版日期:2014-10-01 发布日期:2014-10-10
通讯作者: LEI Zhong-ren, Tel: +86-10-62815930-801, Fax: +86-10-62815930, E-mail: zrlei@ippcaas.cn
作者简介:WANG Hai-hong, Mobile: 18600942206, E-mail: hhwang@ippcaas.cn
基金资助:
This research is partially funded by the National Natural Science Foundation of China (31201526), the National 973 Program of China (2009CB119000), the Earmarked Fund for Modern Agro- Industry Technology Research System (CARS-25-B-07) and the Special Fund for Agro-Scientific Research in the Public Interest of China (20090332).

The mRNA Expression Profiles of Five Heat Shock Protein Genes from Frankliniella occidentalis at Different Stages and Their Responses to Temperatures and Insecticides

WANG Hai-hong, Stuart R Reitz, WANG Li-xia, WANG Shuai-yu, LI Xue , LEI Zhong-ren

1、State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences,
Beijing 100193, P.R.China
2、Malheur County Extension, Oregon State University, Ontario 97914, USA
3、The General Station of Plant Protection in Shandong, Jinan 250100, P.R.China

Received:2013-07-02 Online:2014-10-01 Published:2014-10-10
Contact: LEI Zhong-ren, Tel: +86-10-62815930-801, Fax: +86-10-62815930, E-mail: zrlei@ippcaas.cn
About author:WANG Hai-hong, Mobile: 18600942206, E-mail: hhwang@ippcaas.cn
Supported by:
This research is partially funded by the National Natural Science Foundation of China (31201526), the National 973 Program of China (2009CB119000), the Earmarked Fund for Modern Agro- Industry Technology Research System (CARS-25-B-07) and the Special Fund for Agro-Scientific Research in the Public Interest of China (20090332).

摘要/Abstract

摘要： The western flower thrips, Frankliniella occidentalis (Pergande) is a highly invasive pest that is able to exploit many crops across a wide range of environmental conditions. Five full-length cDNAs of heat shock protein (HSP) genes (Fo-HSP90, Fo-HSP70, Fo-HSP60, Fo-HSP40 and Fo-HSP28.9) were cloned from F. occidentalis, and their expression profiles were investigated under conditions of thermal stress and insecticide exposure, and at different stages during development, using real-time quantitative PCR. All five gene sequences showed high similarity to homologs in other species, indicating the conserved function of this gene family. HSP60 represents an informative phylogenetic marker at the ordinal taxonomic level within Insecta, but HSP90, which has two homologous copies in Hymenoptera, was not informative. The expression of Fo-HSPs under thermal stress suggests that Fo-HSP90, Fo-HSP70, and Fo-HSP28.9 are inducible by both cold and heat stress, Fo-HSP40 is only heat-inducible, and Fo-HSP60 is thermally insensitive. There were two patterns of cold induction of Fo-HSPs: one is from 0 to 4°C and the other is around -8°C. All five Fo-HSPs genes were induced by exposure to sublethal concentrations of the insecticide avermectin. The expression of the five Fo-HSPs during different developmental stages suggests that they all play a role in development of F. occidentalis.

关键词: Frankliniella occidentalis , heat shock protein genes , environmental stress , development , expression profile

Abstract: The western flower thrips, Frankliniella occidentalis (Pergande) is a highly invasive pest that is able to exploit many crops across a wide range of environmental conditions. Five full-length cDNAs of heat shock protein (HSP) genes (Fo-HSP90, Fo-HSP70, Fo-HSP60, Fo-HSP40 and Fo-HSP28.9) were cloned from F. occidentalis, and their expression profiles were investigated under conditions of thermal stress and insecticide exposure, and at different stages during development, using real-time quantitative PCR. All five gene sequences showed high similarity to homologs in other species, indicating the conserved function of this gene family. HSP60 represents an informative phylogenetic marker at the ordinal taxonomic level within Insecta, but HSP90, which has two homologous copies in Hymenoptera, was not informative. The expression of Fo-HSPs under thermal stress suggests that Fo-HSP90, Fo-HSP70, and Fo-HSP28.9 are inducible by both cold and heat stress, Fo-HSP40 is only heat-inducible, and Fo-HSP60 is thermally insensitive. There were two patterns of cold induction of Fo-HSPs: one is from 0 to 4°C and the other is around -8°C. All five Fo-HSPs genes were induced by exposure to sublethal concentrations of the insecticide avermectin. The expression of the five Fo-HSPs during different developmental stages suggests that they all play a role in development of F. occidentalis.

Key words: Frankliniella occidentalis , heat shock protein genes , environmental stress , development , expression profile

WANG Hai-hong, Stuart R Reitz, WANG Li-xia, WANG Shuai-yu, LI Xue , LEI Zhong-ren. The mRNA Expression Profiles of Five Heat Shock Protein Genes from Frankliniella occidentalis at Different Stages and Their Responses to Temperatures and Insecticides[J]. Journal of Integrative Agriculture, 2014, 13(10): 2196-2210.

参考文献

Bettencourt B R, Hogan C C, Nimali M, Drohan B W. 2008.Inducible and constitutive heat shock gene expressionresponds to modification of Hsp70 copy number inDrosophila melanogaster but does not compensate for lossof thermo tolerance in Hsp70 null flies. BMC Biology, 6, 5.

Bielza P. 2008. Insecticide resistance management strategiesagainst the western flower thrips, Frankliniella occidentalis.Pest Management Science, 64, 1131-1138

Bond J A, Bradley B P 1997. Resistance to malathion in heatshockedDaphnia magna. Environmental Toxicology andChemistry, 16, 705-712.

Brocchieri L, Karlin S. 2000. Conservation among HSP60sequences in relation to structure, function, and evolution.Protein Science, 9, 476-486

Broughton S, Herron G A. 2007. Frankliniella occidentalis(Pergande) (Thysanoptera: Thripidae) chemical control:Insecticide efficacy associated with the three consecutivespray strategy. Australian Journal of Entomology, 46,140-145

Brødsgaard H F. 1993. Cold hardiness and tolerance tosubmergence in water in Frankliniella occidentalis(Thysanoptera: Thripidae). Environmental Entomology,22, 647-653

Buchner J. 1999. Hsp90 & Co.-a holding for folding. Trendsin Biochemical Sciences, 24, 136-141

Cheng M Y, Hartl F U, Martin J, Pollock R A, Kalousek F,Neuper W, Hallberg E M, Hallberg R L, Horwich A L.1989. Mitochondrial heat-shock protein hsp60 is essentialfor assembly of proteins imported into yeast mitochondria.Nature, 337, 620-625

Clark M, Worland M R. 2008. How insects survive the cold:Molecular mechanisms-a review. Journal of ComparativePhysiology B (Biochemical Systemic and EnvironmentalPhysiology), 178, 917-933

Colinet H, Lee S F, Hoffman A. 2010. Temporal expressionof heat shock genes during cold stress and recovery fromchill coma in adult Drosophila melanogaster. The FEBSJournal, 277, 174-185

Del Bene G, Dallai R, Marchini D. 1991. Ultrastructure ofthe midgut and the adhering tubular salivary glands ofFrankliniella occidentalis (Pergande) (Thysanoptera:Thripidae). International Journal of Insect Morphologyand Embryology, 20, 15-24

Didomenico B J, Bugaisky G E, Lindquist S. 1982. The heatshock response is self-regulated at both the transcriptionaland posttranscriptional levels. Cell, 31, 593-603

Du Y, Ma C S, Zhao Q H, Yang H P. 2007. Effects of heatstress on physiological and biochemical mechanisms ofinsects: a literature review. Acta Ecologica Sinica, 27,1565-1572

(in Chinese) Espinosa P J, Contreras J, Quint V, Gravalos C, FernandezE, Bielza P. 2005. Metabolic mechanisms of insecticideresistance in the western flower thrips, Frankliniellaoccidentalis (Pergande). Pest Management Science, 61,1009-1015

Fan C Y, Lee S, Cyr D M. 2003. Mechanisms for regulationof Hsp70 function by Hsp40. Cell Stress & Chaperone,8, 309-316

Feder M E, Hofmann G E. 1999. Heat-shock proteins, molecularchaperones, and the stress response: Evolutionary andecological physiology. Annual Review of Physiology, 61,243-282

Feng H, Liu Y, He L, Yang D, Li M, Lu W. 2008. Heat shockresponse and hsps of Tetranychus cinnabarinus (Acari:Tetranychidae) resistant to avermectin. Acta EcologicaSinica, 51, 1235-1242 (in Chinese)

Feng H, Wang L, Liu Y, He L, Li m, Lu W, Xue C. 2010.Molecular characterization and expression of a heat shockprotein gene (HSP90) from the carmine spider mite,Tetranychus cinnabarinus (Boisduval). Journal of InsectScience, 10, 112.

Fujikake N, Nagai Y, Popiel H A, Kanoa H, YamaguchiM, Todaa T. 2005. Alternative splicing regulatesthe transcriptional activity of Drosophila heat shocktranscription factor in response to heat/cold stress. FEBSLetters, 579, 3842-3848

Gai H T, Zhi J R, Li Z X, Jiang Y J 2010. Survival rates ofFrankliniella occidentalis and Frankliniella intonsa afterexposure to adverse temperature conditions. ChineseJournal of Ecology, 29, 1533-1537 (in Chinese)

Gao Y, Lei Z, Reitz S R. 2012. Western flower thrips resistanceto insecticides: Detection, mechanisms and managementstrategies. Pest Management Science, 68, 1111-1121

Gehring W J, Wehner R. 1995. Heat shock protein synthesisand thermotolerance in cataglyphis, an ant from the saharadesert. Proceedings of the National Academy of Sciencesof the United States of America, 92, 2994-2998

Gething M J, Sambrook J. 1992. Protein folding in the cell.Nature, 353, 33-45

Giese K C, Vierling E. 2004. Mutants in a small heat shockprotein that affect the oligomeric state. Analysis and allelespecificsuppression. The Journal of Biological Chemistry,279, 32674-32683

Gkouvitsas T, Kontogiannatos D, Kourti A. 2009. Expressionof the Hsp83 gene in response to diapause and thermalstress in the moth Sesamia nonagrioides. Insect MolecularBiology, 18, 759-768

Gu X, Tian S, Wang D, Gao F. 2009. Interaction betweenshort-term heat pretreatment and avermectin on 2nd instarlarvae of diamondback moth, Plutella xylostella (Linn).Dose-Response, 7, 270-283

Gupta R S. 1995. Phylogenetic analysis of the 90 kD heatshock family of protein sequences and an examination ofthe relationship among animals, plants, and fungi species.Molecular Biology and Evolution, 12, 1063-1073

Gupta S C, Siddique H R, Mathur N, Mishra R K, Saxena D K,Chowdhuri D K. 2007a. Adverse effect of organophosphatecompounds, dichlorvos and chlorpyrifos in the reproductivetissues of transgenic Drosophila melanogaster: 70 kDa heatshock protein as a marker of tissues of cellular damage.Toxicology, 238, 1-14

Gupta S C, Siddique H R, Mathur N, Vishwakarma A L, MishraR K, Saxena D K, Chowdhuri D K. 2007b. Induction ofhsp70, alteration in oxidative stress markers and apoptosidagainst dichlorvos exposure in transgenic Drosophilamelanogaster: modulation by reactive oxygen species.Biochimica et Biophysica Acta, 1770, 1382-1394

Haass C, Klein U, Kloetzel P M. 1990. Developmentalexpression of Drosophila melanogaster small heat-shockproteins. Journal of Cell Science, 96, 413-418

He L, Xue C H, Zhao Z M, Wang J J. 2008. Relative fitnessof Tetranychus cinnabarinus resistant strains at differenttemperatures. The Journal of Applied Ecology, 19, 2449-2454 (in Chinese)

Heming B S. 1973. Metamorphosis of the pretarsus inFrankliniella fusca (Hinds) (Thripidae) and Haplothripsverbasci (Oosborn) (Phlaeothripidae) (Thysanoptera).Canadian Journal of Zoology, 51, 1211-1234

Herron G A, Rophail J, Gullick G C. 1996. Laboratory-based,insecticide efficacy studies on field-collected Frankliniellaoccidentalis (Pergande) (Thysanoptera: Thripidae) andimplications for its management in Australia. AustralianJournal of Entomology, 35, 161-164

Huang L H, Kang L. 2007. Cloning and interspecific alteredexpression of heat shock protein genes in two leafminerspecies in response to thermal stress. Insect MolecularBiology, 16, 491-500

Huang L H, Wang C Z, Kang L. 2009. Cloning and expressionof five heat shock protein genes in relation to old hardeningand development in the leafminer, Liriomyza sativa.Journal of Insect Physiology, 55, 279-285

Immaraju J A, Paine T D, Bethke J A, Robb K L, Newman JP. 1992. Western flower thrips (Thysanoptera: Thripidae)resistance to insecticides in coastal California greenhouses.Journal of Economic Entomology, 85, 9-14

Jaya N, Garcia V, Vierling E. 2009. Substrate binding siteflexibility of the small heat shock protein molecularchaperones. Proceedings of the National Academy ofSciences of the United States of America, 106, 15604-15609

Jiang X, Zhai H, Wang L, Luo L, Sappington T W, ZhangL. 2012. Cloning of the heat shock protein 90 and 70genes from the beet armyworm, Spodoptera exigua, andexpression characteristics in relation to thermal stress anddevelopment. Cell Stress & Chaperones, 17, 67-80

Joanisse D R, Michaud S, Inaguma Y, Tanguay R M. 1998.Small heat shock proteins of Drosophila: Developmentalexpression and functions. Journal of Biosciences, 23,369-376

Kalosaka K, Soumaka E, Politis N, Mintzas A C. 2009.Thermotolerance and HSP70 expression in theMediterrancan fruit fly Ceratitis capitata. Journal of Insect Physiology, 55, 568-573

Kay I R, Herron G A. 2010. Evaluation of existing and newinsecticides including spirotetramat and pyridalyl to controlFrankliniella occidentalis (Pergande) (Thysanopterra:Thripidae) on peppers in Queensland. Australian Journalof Entomology, 49, 175-181

Kirk W D J, Terry L I. 2003. The spread of the western flowerthrips Frankliniella occidentalis (Pergande). Agriculturaland Forest Entomology, 5, 301-310

Knowlton A A, Salfity M. 1996. Nuclear localization and theheat shock proteins. Journal of Bioscience, 21, 123-142

Kontsedalov S Weintraub P G, Horowitz A R, Ishaaya I. 1998.Effects of insecticides on immature and adult westernflower thrips (Thysanoptera: Thripidae) in Israel. Journalof Economic Entomology, 91, 1067-1071

Kregel K C. 2002. Heat shock proteins: Modifyingfactors in physiological stress responses and acquiredthermotolerance. Journal of Applied Physiology, 92,2177-2186

Li H B, Shi L, Wang J J, Du Y Z. 2011a. Impact of temperaturehardening on thermal tolerance and reproduction inFrankliniella occidentalis. Chinese Journal of AppliedEntomology, 48, 530-535

(in Chinese)Li H B, Shi L, Wang J J, Du Y Z. 2011b. Rapid cold hardengingof western flower thrips, Frankliniella occidentalis, andits ecological cost. Acta Ecologica Sinica, 31, 7196-7202(in Chinese)

Li Y P. 2012. Research on technology to control thrips withthe entomopathogenic fungus, Beauveria bassiana. MScthesis, Chinses Academy of Agricultural Science, Beijing.(in Chinese)

Liang X H, Lei Z R, Wen J Z, Zhu M L. 2010. The diurnal flightactivity and influential factors of Frankliniella occidentalisin the greenhouse. Insect Science, 17, 535-541

Mahroof R, Yan Zhu K, Subramanam B, Bai J. 2005.Expression patterns of three heat shock protein 70 genesamong developmental stages of the red flour beetle,Tribolium castaneum (Coleoptera: Tenebrionidae).Comparative Biochemistry and Physiology (Part A,Molecular & Integrative Physiology), 141, 247-256

Martin J, Horwich A L, Hartl F U. 1992. Prevention of proteindenaturation under heat stress by the chaperonin Hsp60.Science, 258, 995-998

McDonald J R, Bale J S, Walters K F A. 1997. Effects of sublethalcold stress on the western flower thrips, Frankliniellaoccidentalis. Annals of Applied Biology, 131, 189-195

McDonald J R, Bale J S, Walters K F A. 1997. Low temperaturemortality and overwintering of the western flower thripsFrankliniella occidentalis (Thysanoptera: Thripidae).Bulletin of Entomological Research, 87, 497-505

McDonald J R, Bale J S, Walters K F A. 1997. Rapid coldhardening in the western flower thrips Frankliniellaoccidentalis. Journal of Insect Physiology, 43, 759-776

Morrow G, Samson M, Michaud S, Tanguay R M. 2004.Overexpression of the small mitochondrial hsp22 extendsDrosophila life span and increases resistance to oxidativestress. The FASEB Journal, 18, 598-599

Morse J G, Hoddle M S. 2006. Invasion biology of thrips.Annuall Review of Entomology, 51, 67-89

Pfaffl M W. 2001. A new mathematical model for relativequantification in real-time RT-PCR. Nucleic AcidsResearch, 29, e45.

Poulain P, Gelly J C, Flatters D. 2010. Detection andarchitecture of small heat shock protein monomers. PLoSONE, 5, e9990.

Qian Y Q, Patel D, Hartl F U, McColl D J. 1996. Nuclearmagnetic resonance solution structure of the human Hsp40 (HDJ-1) J-domain Journal of Molecular Biology, 260,224-235

Qiu X B, Shao Y M, Miao S,Wang L. 2006. The diversityof the DnaJ/Hsp40 family, the crucial partners for Hsp70chaperones. Cellular and Molecular Life Sciences, 63,2560-2570

Raghavendra K, Barik T K, Adak T. 2010. Development oflarval thermotolerance and impact on adult susceptibilityto malathion insecticide and Plasmodium vivax infectionin Anopheles stephensi. Parasitology Research, 107,1291-1297

Ramsey A J, Russell L C, Whitt S R, Chinkers M. 2000.Overlapping sites of tetratricopeptide repeat proteinblinding and chaperone activity in heat shock protein 90.The Journal of Biological Chemistry, 275, 17857-17862

Reitz S R. 2009. Biology and ecology of the western flowerthrips (Thysanoptera: Thripidae): The making of a pest.Florida Entomologist, 92, 7-13

Reitz S R, Gao Y L, Lei Z R. 2011. Thrips: Pest of concernto china and the united states. Journal of IntegratiaveAgriculture, 10, 867-892

Rotenberg D, Whitfield A E. 2010. Analysis of expressedsequence tags for Frankliniella occidentalis, the westernflower thrips. Insect Molecular Biology, 19, 537-551

Saraste M, Sibbald P R, Wittinghofer A. 1990. The P-loop-acommon motif in ATP and GTP-binding proteins. Trendsin Biochemical Sciences, 15, 430-434

Scheufler C, Brinker A, Bourenkov G, Pegoraro S, MoroderL, Bartunik H, Hartl F U, Moarefi I. 2000. Structure ofTPR domain-peptide complexes: Critical elements in theassembly of the Hsp70-Hsp90 multichaperone machine.Cell, 101, 199-210

Sharma S, Reddy P V J, Rohilla M S,Tiwari P K. 2006.Expression of hsp60 homologue in sheep blowfly Luciliacuprina during development and heat stress. Journal ofThermal Biology, 31, 1546-555

Sharma S, Rohilla M S, Reddy P V, Tiwari P K. 2008. In vitroinduction of 60-kDa and 70-kDa heat shock proteins byendosulphan and monocrotophos in sheep blowfly Luciliacuprina. Archive of Environmental Contamination andToxicology, 55, 57-69

Shen Y, Gu J, Huang L H, Zheng S C, Liu L, Xu W H, FengQ L, Kang L. 2011. Cloning and expression analysis of sixsmall heat shock protein genes in the common cutworm,Spodoptera litura. Journal of Insect Physiology, 57, 908- 914.Sinclair B J, Gibbs A G, Roberts S P. 2007. Gene transcriptionduring exposure to, and recovery from, cold anddesiccation stress in Drosophila melanogaster. InsectMolecular Biology, 16, 435-443

Sørensen J G, Kristensen T N, Loeschcke V. 2003. Theevolutionary and ecological role of heat shock proteins.Ecology Letters, 6, 1025-1037

Sørensen J G, Loeschcke V. 2007. Studing stress responses inthe post-genomic era: its ecological and evolutionary role.Journal of Biosciences, 32, 447-456

Stechmann A, Cavalier-Smith T. 2003. Phylogenetic analysisof eukaryotes using heat-shock protein Hsp90. Journal ofMolecular Evolution, 57, 408-419

van der Straten A, Rommel C, Dickson B, Hafen E. 1997.The heat shock protein 83 (Hsp83) is required for Rafmediatedsignaling in the Drosophila. EMBO Journal,16, 1961-1969

Takahashi K, Rako L, Takano-Shimizu T, Hoffmann A, LeeS. 2010. Effects of small Hsp genes on developmentalstability and microenvironmental canalization. BMCEvolutionary Biology, 10, 284.Tamura K, Dudley J, Nei M, Kumar S. 2007. Mega4: Molecularevolutionary genetics analysis (MEGA) software version4.0. Molecular Biology and Evolution, 24, 1596-1599

Theodoraki M A, Mintzas A C. 2006. cDNA cloning, heatshock regulation and developmental expression of thehsp83 gene in the Mediterranean fruit fly Ceratitis capitata.Insect Molecular Biology, 15, 839-852

Thompson J D, Gibson T J, Plewniak F, Jeanmougin F, HigginsD G. 1997. The Clustal X windows interace: Flexiblestrategies for multiple sequence alignment aided by qualityanalysis tools. Nucleic Acids Research, 25, 4876-4882

Ullman D E, Meidero R, Campbell L R, Whitfield A E,Sherwood J L, German T L. 2002. Thrips as vectors oftospoviruses. Advances in Botanical Research, 36, 113-140

Ullman D E, Westcott D M, Hunter W B, Mau R F L. 1989.Internal anatomy and morphology of Frankliniellaoccidentalis (Pergande) (Thysanopter: Thripidae) withspecial reference to interactions between thrips andtomato spotted wilt virus. International Journal of InsectMorphology and Embryology, 18, 289-310

Vandesompele J, Depreter K, Pattyn F, poppe B, van Roy N,de Paepe A, Speleman F. 2002. Accurate normalizationof real-time quantitative RT-PCR data by geometricaveraging of multiple internal control genes. GenomeBiology, 3, doi: 10.1186/gb-2002-3-7-research0034Wang H, Lei Z, Li X, Oetting R D 2011. Rapid cold hardeningand expression of heat shock protein genes in the B-biotypeBemisia tabaci. Environmental Entomology, 40, 132-139

Xu P, Xiao J, Liu L, Li T, Huang D. 2010. Molecular cloningand characterization of four heat shock protein genesfrom Macrocentrus cingulum (Hymenoptra: Braconidae).Molecular Biology Reports, 37, 2265-2272

Yang L H, Jiang H B, Liu Y H, Dou W, Wang J J. 2012.Molecular characterization of three heat shock protein 70genes and their expersssion profiles under thermal stressin the citrus red mite. Molecular Biology Reports, 39,3585-3596

Yue L, Karr T L, Nathan D F, Swift H, Srinivasan S, LindquistS. 1999. Genetic analysis of viable Hsp90 alleles revealsa critical role in Drosophila spermatogenesis. Genetics,151, 1065-1079

Zhao S, Fernald R D. 2005. Comprehensive algorithm forquantitative real-time polymerase chain reaction. Journalof Computational Biology, 12, 1047-1064.

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The mRNA Expression Profiles of Five Heat Shock Protein Genes from Frankliniella occidentalis at Different Stages and Their Responses to Temperatures and Insecticides

The mRNA Expression Profiles of Five Heat Shock Protein Genes from Frankliniella occidentalis at Different Stages and Their Responses to Temperatures and Insecticides

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