瓜实蝇热激蛋白Hsp90基因克隆及表达分析
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摘要
【目的】热激蛋白基因Hsps在生物体抗逆性过程中具有重要的作用,本文旨在通过阐释瓜实蝇Bactrocera cucurbitae (Coquillett)热激蛋白基因Hsp90在其对环境温度适应性及抗药性过程中的功能作用,为瓜实蝇综合治理提供理论基础。【方法】采用RACE-PCR技术克隆瓜实蝇的Hsp90基因cDNA序列,利用生物信息学工具分析序列特征,并通过实时定量PCR技术分析高温胁迫、阿维菌素诱导和抗性及敏感品系中该基因的表达情况。【结果】克隆获得的瓜实蝇Hsp90基因cDNA全长2 654 bp,命名为Bc-Hsp90,GenBank登录号为KP864677,含2 145 bp的开放阅读框,编码715个氨基酸蛋白,具有HSP90蛋白家族共有模式和1个基序标签,C-末端具有MEEVD基序,属于胞质型热激蛋白。系统发育分析显示,Bc-Hsp90基因高度保守。不同高温(32-40℃)胁迫处理1 h和2 h后,瓜实蝇成虫体内Bc-Hsp90的相对表达量均显著高于对照组(26℃),并在38℃和40℃表达量最高;阿维菌素长期筛选的RS品系,Bc-Hsp90表达量是对照SS品系的2.13倍,但RS品系以LC90剂量诱导后,Bc-Hsp_(90)表达量显著下调,随着恢复时间延长其表达量逐渐升高,96 h后恢复到对照水平。【结论】推测Bc-Hsp90在瓜实蝇耐热性和抗阿维菌素过程中可能起着重要作用。
[Objectives] To investigate the function of the heat shock protein Hsp90 gene of Bactrocera cucurbitae(Coquillett)(Bc-Hsp90) under different temperatures and pesticide stress in order to improve control of this pest. [Methods]The cDNA full-length fragment of the Bc-Hsp90 was cloned using the RACE-PCR method. Bioinformatics tools were used to analyze the sequence characteristics, and real-time quantitative PCR was used to detect the expression levels of the gene under heat stress, and after exposure to the pesticide abamectin, in abamectin-resistant and susceptible strains. [Results] The complete sequence of 2 654 bp was obtained(Accession number: KP864677) and was found to contain a 2 145 bp open reading frame(ORF) encoding 715 amino acids. Family signatures of the HSP90 protein and the cytoplasm of the Hsp90 gene C-terminal region MEEVD motif were detected. Phylogenetic analysis indicates that Bc-Hsp90 is highly conserved. Real-time quantitative PCR results showed that 1 h and 2 h of heat stress(32-40℃)up-regulated the expression of Bc-Hsp90. Expression peaked at 38℃ and 40℃ and expression in an abamectin resistant strain(RS) was 2.13 times higher than in a sensitive strain(SS). The expression of the Bc-Hsp90 gene was down-regulated after exposure to an LC_(90) dose of abamectin and returned to normal levels after 96 h. [Conclusion] The expression level of Bc-Hsp90 could play an important role in heat resistance and pesticide tolerance in B. cucurbitae.
[Objectives] To investigate the function of the heat shock protein Hsp90 gene of Bactrocera cucurbitae(Coquillett)(Bc-Hsp90) under different temperatures and pesticide stress in order to improve control of this pest. [Methods]The cDNA full-length fragment of the Bc-Hsp90 was cloned using the RACE-PCR method. Bioinformatics tools were used to analyze the sequence characteristics, and real-time quantitative PCR was used to detect the expression levels of the gene under heat stress, and after exposure to the pesticide abamectin, in abamectin-resistant and susceptible strains. [Results] The complete sequence of 2 654 bp was obtained(Accession number: KP864677) and was found to contain a 2 145 bp open reading frame(ORF) encoding 715 amino acids. Family signatures of the HSP90 protein and the cytoplasm of the Hsp90 gene C-terminal region MEEVD motif were detected. Phylogenetic analysis indicates that Bc-Hsp90 is highly conserved. Real-time quantitative PCR results showed that 1 h and 2 h of heat stress(32-40℃)up-regulated the expression of Bc-Hsp90. Expression peaked at 38℃ and 40℃ and expression in an abamectin resistant strain(RS) was 2.13 times higher than in a sensitive strain(SS). The expression of the Bc-Hsp90 gene was down-regulated after exposure to an LC_(90) dose of abamectin and returned to normal levels after 96 h. [Conclusion] The expression level of Bc-Hsp90 could play an important role in heat resistance and pesticide tolerance in B. cucurbitae.
引文
Ansari MS,Hasan F,Ahmad N,2012.Threats to fruit and vegetable crops:fruit flies(Tephritidae)-ecology,behaviour,and management.Journal of Crop Science&Biotechnology,15(3):169-188.
Chen H,Xu X,Li Y,Wu J,2014.Characterization of heat shock protein 90,70 and their transcriptional expression patterns on high temperature in adult of Grapholita molesta(Busck).Insect Science,21(4):439-448.
Dhillon MK,Singh R,Naresh JS,Sharma HC,2005.The melon fruit fly,Bactrocera cucurbitae:A review of its biology and management.Journal of Insect Science,5(1).Doi:10.1093/jis/5.1.40.
Dupuis JR,Sim SB,Jose MS,Leblanc L,Hoassain MA,Rubinoff D,Geib SM,2018.Population genomics and comparisons of selective signatures in two invasions of melon fly,Bactrocera cucurbitae(Diptera:Tephritidae).Biological Invasions,20(5):1211-1228.
Feng HZ,Liu YH,He L,Li M,Lu RE,2010.Cross tolerance of carmine spider mite,Tetrany chus cinnabarinus,to abamectin and high temperature.Journal of Zhejiang University(Agric.&Life Sci.),36(2):159-167.[冯宏祖,刘映红,何林,李明,陆蕊娥,2010.朱砂叶螨对阿维菌素及高温的交互耐性.浙江大学学报(农业与生命科学版),36(2):159-167.]
Gu SW,Zeng L,Liang GW,2015.Monitoring for insecticide resistance of melon fly populations in the field of Southern China.Journal of South China Agricultural University,36(4):76-80.[谷世伟,曾玲,梁广文,2015.华南地区瓜实蝇田间种群的抗药性监测.华南农业大学学报,36(4):76-80.]
Guo XJ,Feng JN,2018.Comparisons of expression levels of heat shock proteins(hsp70 and hsp90)from Anaphothrips obscurus(Thysanoptera:Thripidae)in polymorphic adults exposed to different heat shock treatments.Journal of Insect Science,18(3).Doi:10.1093/jisesa/iey059.
Guo YJ,Liang P,Gao XW,2013.Induced expression of hsp70m RNA by nitenpyram,chlorpyrifos and beta-cypermethrin in Bemisia tabaci Mediterranean(Hemiptera:Aleyrodidae).Acta Entomologica Sinica,56(1):29-38.[郭雅洁,梁沛,高希武,2013.烯啶虫胺、毒死蜱和高效氯氰菊酯对烟粉虱地中海隐种hsp70 mRNA的诱导表达.昆虫学报,56(1):29-38.]
Hsu JC,Haymer DS,Chou MY,Feng HT,Chen HH,Huang YB,Mau RFL,2012.Monitoring resistance to spinosad in the melon fly(Bactrocera cucurbitae)in Hawaii and Taiwan.The Scientific World Journal,2012:Article ID 750576.8.
Kong LB,Lin W,Li ZH,Wan FH,Wang ZL,Huang GS,2008.Apredication of potential geographic distribution of melon fruit fly based on CLIMEX and DIVA-GIS.Journal of Plant Protection,35(2):148-154.[孔令斌,林伟,李志红,万方浩,王之岭,黄冠胜,2008.基于CLIMEX和DIVA-GIS的瓜实蝇潜在地理分布预测.植物保护学报,35(2):148-154.]
Li J,Qian X,Sha B,2009.Heat shock protein 40:structural studies and their functional implications.Protein&Peptide Letters,16(6):606-612.
Li YT,Zhao Q,Fang B,Chen MH,2017.Molecular cloning and expression analysis of the Hsp90 gene in the bird cherry-oat aphid,Rhopalosiphum padi.Journal of Plant Protection,44(1):16-23.[李玉婷,赵奇,房冰,陈茂华,2017.禾谷缢管蚜热激蛋白Hsp90基因的克隆和表达分析.植物保护学报,44(1):16-23.]
Matthew SS,Jang EB,2010.Cucumber volatile blend attractive to female melon fly,Bactrocera cucurbitae(Coquillett).Journal of Chemical Ecology,36(7):699-708.
Morimoto RI,Kline MP,Bimston DN,Cotto JJ,1997.The heat-shock response:regulation and function of heat-shock proteins and molecular chaperones.Essays in Biochemistry,32:17-29.
Parsell DA,Lindquist S,1993.The function of heat-shock proteins in stress tolerance-degradation and reaction of damageproteins.Annual Review of Genetics,27:437-496.
Ren ZC,Wu WJ,Li Mh,Fu YG,2013.Screening of attraction formula for male Bactrocera cucurbitae in laboratory and field.Chinese Journal of Tropical Crops,34(4):743-746.[任志超,吴伟坚,李梅辉,符悦冠,2013.瓜实蝇雄虫引诱剂配方的筛选.热带作物学报,34(4):743-746.]
Ritossa F,1962.A new puffing pattern induced by temperature shock and DNP in drosophila.Cellular and Molecular Life Sciences,18(12):571-573.
Roy S,Prasad A,Handique G,Barua A,2016.First report on heat shock protein expression in red spider mites(Oligonychus coffeae)in response to pesticide exposure.Invertebrate Survival Journal,13:350-354.
Rutherford SL,Lindquist S,1998.Hsp90 as a capacitor for morphological evolution.Nature,396(6709):336-342.
Shen JR,Li MF,Chen NZ,Wang JJ,Wan FH,2011.Cloning and analysis of the expression characteristics under heat stress of Hsp90 gene in the codling moth,Cydia pomonella(Lepidoptera:Tortricidae).Acta Entomologica Sinica,54(11):1236-1248.[申建茹,李明福,陈乃中,王进军,万方浩,2011.苹果蠹蛾热激蛋白Hsp90基因的克隆及热胁迫下的表达分析.昆虫学报,54(11):1236-1248.]
S?rensen JG,Kristensen TN,Loeschcke V,2010.The evolutionary and ecological role of heat shock proteins.Ecology Letters,6(11):1025-1037.
Sun Y,Sheng Y,Bai L,Zhang Y,Xiao Y,Xiao L,Tan Y,Shen Y,2014.Characterizing heat shock protein 90 gene of Apolygus lucorum(Meyer-Dür)and its expression in response to different temperature and pesticide stresses.Cell Stress and Chaperones,19(5):725-739.
Theodoraki MA,Mintzas AC,2006.c DNA cloning,heat shock regulation and developmental expression of the hsp83 gene in the Mediterranean fruit fly Ceratitis capitata.Insect Molecular Biology,15(6):839-852.
Tian H,Yu S,Liu B,Yang J,Li X,Yue J,Chen F,Ding L,Liu H,Li H,2015.Molecular cloning of heat shock protein gene HSP90and effects of abamectin and double-stranded RNA on its expression in Panonychus citri(Trombidiformes:Tetranychidae).Florida Entomologist,98(1):37-43.
Tissières A,Mitchell HK,Tracy UM,1974.Protein synthesis in salivary glands of Drosophila melanogaster:relation to chromosome puffs.Journal of Molecular Biology,84(3):389-398.
Tungjitwitayakul J,Tatun N,Vajarasathira B,Sakurai S,2015.Expression of heat shock protein genes in different developmental stages and after temperature stress in the maize weevil(Coleoptera:Curculionidae).Journal of Economic Entomology,108(3):1313-1323.
Vontas J,Hernández-Crespo P,Margaritopoulos JT,Ortego F,Feng HT,Mathiopoulos KD,Hsu JC,2011.Insecticide resistance in Tephritid flies.Pesticide Biochemistry&Physiology,100(3):199-205.
Wang FY,Yang L,Li LF,Liao SC,Liao RZ,2018.Selection of reference genes in the Bactrocera cucurbitae(Coquillett)under temperature stress by RT-qPCR.Journal of Environmental Entomology,40(5):1097-1105.[王凤英,杨朗,黎柳锋,廖世纯,廖仁昭,姜建军,2018.不同温度胁迫下瓜实蝇RT-qPCR内参基因筛选.环境昆虫学报,40(5):1097-1105.]
Wang HH,Reitz SR,Wang LX,Wang SY,Li X,Lei ZR,2014.The m RNA expression profiles of five heat shock protein genes from Frankliniella occidentalis at different stages and their responses to temperatures and insecticides.Journal of Integrative Agriculture,13(10):2196-2210.
Wang LD,Shan D,Yao J,Fang JC,2015.Induced expression of the heat shock protein 70 and 90 genes by exposure to high temperature and chlorpyrifosin female of Lanodelphax striatellus.Chinese Journal of Applied Entomology,52(4):828-836.[王利华,单丹,姚静,方继朝,2015.温度和毒死蜱对灰飞虱雌成虫热激蛋白70和90基因的诱导表达特性研究.应用昆虫学报,52(4):828-836.]
Wang QX,Li ZY,Xie Y,Cao H,2008.Research progress of heat shock proteins in Drosophila.Chinese Bulletin of Entomology,45(5):698-702.[王秋香,李宗芸,谢艳,曹慧,2008.果蝇热激蛋白的研究进展.昆虫知识,45(5):698-702.]
Wu YK,Zou C,Fu DM,Zhang WN,Xiao HJ,2018.Molecular characterization of three Hsp90 from Pierisand expression patterns in response to cold and thermal stress in summer and winter diapause of Pieris melete.Insect Science,25(2):273-283.
Yang J,Nasir AB,Fan D,2017.cDNA Cloning and induction of heat shock protein Hsp90 from Mythimna separata.Chinese Journal of Biological Control,33(5):623-630.[杨静,Baloch Nasir Ali,樊东,2017.黏虫热休克蛋白Hsp90基因的克隆及不同温度对其诱导反应.中国生物防治学报,33(5):623-630.]
Yang LH,Dou W,Jiang HB,Niu JZ,Ding TB,Wang JJ,2016.Cloning and expression profiling of heat shock protein gene Pc Hsp90 in the citrus red mite,Panonychus citri(Acari:Tetranychidae).Acta Entomologica Sinica,59(4):411-420.[杨丽红,豆威,蒋红波,牛金志,丁天波,王进军,2016.柑橘全爪螨热激蛋白基因Pc Hsp90的克隆及表达模式分析.昆虫学报,59(4):411-420.]
Zhang M,Li JC,Liu XX,ZHang QW,ZHao ZW,2009.The relationship between the heat shock protein 90 and the development of Microplitis mediator.Acta Entomologica Sinica,46(2):284-289.[张敏,李建成,刘小侠,张青文,赵章武,2009.热激蛋白90与中红侧沟茧蜂的发育关系.昆虫知识,46(2):284-289.]
Zhang Q,Lu MX,Zhu SD,2014.Cloning,sequence analysis and expression profiling of heat shock protein 90 gene in the small brown plant hopper,Laodelphax striatellus(Hemiptera:Delphacidae).Acta Entomologica Sinica,57(7):777-786.[张青,陆明星,祝树德,2014.灰飞虱热激蛋白Hsp90基因的克隆、序列分析与表达模式.昆虫学报,57(7):777-786.]
Chen H,Xu X,Li Y,Wu J,2014.Characterization of heat shock protein 90,70 and their transcriptional expression patterns on high temperature in adult of Grapholita molesta(Busck).Insect Science,21(4):439-448.
Dhillon MK,Singh R,Naresh JS,Sharma HC,2005.The melon fruit fly,Bactrocera cucurbitae:A review of its biology and management.Journal of Insect Science,5(1).Doi:10.1093/jis/5.1.40.
Dupuis JR,Sim SB,Jose MS,Leblanc L,Hoassain MA,Rubinoff D,Geib SM,2018.Population genomics and comparisons of selective signatures in two invasions of melon fly,Bactrocera cucurbitae(Diptera:Tephritidae).Biological Invasions,20(5):1211-1228.
Feng HZ,Liu YH,He L,Li M,Lu RE,2010.Cross tolerance of carmine spider mite,Tetrany chus cinnabarinus,to abamectin and high temperature.Journal of Zhejiang University(Agric.&Life Sci.),36(2):159-167.[冯宏祖,刘映红,何林,李明,陆蕊娥,2010.朱砂叶螨对阿维菌素及高温的交互耐性.浙江大学学报(农业与生命科学版),36(2):159-167.]
Gu SW,Zeng L,Liang GW,2015.Monitoring for insecticide resistance of melon fly populations in the field of Southern China.Journal of South China Agricultural University,36(4):76-80.[谷世伟,曾玲,梁广文,2015.华南地区瓜实蝇田间种群的抗药性监测.华南农业大学学报,36(4):76-80.]
Guo XJ,Feng JN,2018.Comparisons of expression levels of heat shock proteins(hsp70 and hsp90)from Anaphothrips obscurus(Thysanoptera:Thripidae)in polymorphic adults exposed to different heat shock treatments.Journal of Insect Science,18(3).Doi:10.1093/jisesa/iey059.
Guo YJ,Liang P,Gao XW,2013.Induced expression of hsp70m RNA by nitenpyram,chlorpyrifos and beta-cypermethrin in Bemisia tabaci Mediterranean(Hemiptera:Aleyrodidae).Acta Entomologica Sinica,56(1):29-38.[郭雅洁,梁沛,高希武,2013.烯啶虫胺、毒死蜱和高效氯氰菊酯对烟粉虱地中海隐种hsp70 mRNA的诱导表达.昆虫学报,56(1):29-38.]
Hsu JC,Haymer DS,Chou MY,Feng HT,Chen HH,Huang YB,Mau RFL,2012.Monitoring resistance to spinosad in the melon fly(Bactrocera cucurbitae)in Hawaii and Taiwan.The Scientific World Journal,2012:Article ID 750576.8.
Kong LB,Lin W,Li ZH,Wan FH,Wang ZL,Huang GS,2008.Apredication of potential geographic distribution of melon fruit fly based on CLIMEX and DIVA-GIS.Journal of Plant Protection,35(2):148-154.[孔令斌,林伟,李志红,万方浩,王之岭,黄冠胜,2008.基于CLIMEX和DIVA-GIS的瓜实蝇潜在地理分布预测.植物保护学报,35(2):148-154.]
Li J,Qian X,Sha B,2009.Heat shock protein 40:structural studies and their functional implications.Protein&Peptide Letters,16(6):606-612.
Li YT,Zhao Q,Fang B,Chen MH,2017.Molecular cloning and expression analysis of the Hsp90 gene in the bird cherry-oat aphid,Rhopalosiphum padi.Journal of Plant Protection,44(1):16-23.[李玉婷,赵奇,房冰,陈茂华,2017.禾谷缢管蚜热激蛋白Hsp90基因的克隆和表达分析.植物保护学报,44(1):16-23.]
Matthew SS,Jang EB,2010.Cucumber volatile blend attractive to female melon fly,Bactrocera cucurbitae(Coquillett).Journal of Chemical Ecology,36(7):699-708.
Morimoto RI,Kline MP,Bimston DN,Cotto JJ,1997.The heat-shock response:regulation and function of heat-shock proteins and molecular chaperones.Essays in Biochemistry,32:17-29.
Parsell DA,Lindquist S,1993.The function of heat-shock proteins in stress tolerance-degradation and reaction of damageproteins.Annual Review of Genetics,27:437-496.
Ren ZC,Wu WJ,Li Mh,Fu YG,2013.Screening of attraction formula for male Bactrocera cucurbitae in laboratory and field.Chinese Journal of Tropical Crops,34(4):743-746.[任志超,吴伟坚,李梅辉,符悦冠,2013.瓜实蝇雄虫引诱剂配方的筛选.热带作物学报,34(4):743-746.]
Ritossa F,1962.A new puffing pattern induced by temperature shock and DNP in drosophila.Cellular and Molecular Life Sciences,18(12):571-573.
Roy S,Prasad A,Handique G,Barua A,2016.First report on heat shock protein expression in red spider mites(Oligonychus coffeae)in response to pesticide exposure.Invertebrate Survival Journal,13:350-354.
Rutherford SL,Lindquist S,1998.Hsp90 as a capacitor for morphological evolution.Nature,396(6709):336-342.
Shen JR,Li MF,Chen NZ,Wang JJ,Wan FH,2011.Cloning and analysis of the expression characteristics under heat stress of Hsp90 gene in the codling moth,Cydia pomonella(Lepidoptera:Tortricidae).Acta Entomologica Sinica,54(11):1236-1248.[申建茹,李明福,陈乃中,王进军,万方浩,2011.苹果蠹蛾热激蛋白Hsp90基因的克隆及热胁迫下的表达分析.昆虫学报,54(11):1236-1248.]
S?rensen JG,Kristensen TN,Loeschcke V,2010.The evolutionary and ecological role of heat shock proteins.Ecology Letters,6(11):1025-1037.
Sun Y,Sheng Y,Bai L,Zhang Y,Xiao Y,Xiao L,Tan Y,Shen Y,2014.Characterizing heat shock protein 90 gene of Apolygus lucorum(Meyer-Dür)and its expression in response to different temperature and pesticide stresses.Cell Stress and Chaperones,19(5):725-739.
Theodoraki MA,Mintzas AC,2006.c DNA cloning,heat shock regulation and developmental expression of the hsp83 gene in the Mediterranean fruit fly Ceratitis capitata.Insect Molecular Biology,15(6):839-852.
Tian H,Yu S,Liu B,Yang J,Li X,Yue J,Chen F,Ding L,Liu H,Li H,2015.Molecular cloning of heat shock protein gene HSP90and effects of abamectin and double-stranded RNA on its expression in Panonychus citri(Trombidiformes:Tetranychidae).Florida Entomologist,98(1):37-43.
Tissières A,Mitchell HK,Tracy UM,1974.Protein synthesis in salivary glands of Drosophila melanogaster:relation to chromosome puffs.Journal of Molecular Biology,84(3):389-398.
Tungjitwitayakul J,Tatun N,Vajarasathira B,Sakurai S,2015.Expression of heat shock protein genes in different developmental stages and after temperature stress in the maize weevil(Coleoptera:Curculionidae).Journal of Economic Entomology,108(3):1313-1323.
Vontas J,Hernández-Crespo P,Margaritopoulos JT,Ortego F,Feng HT,Mathiopoulos KD,Hsu JC,2011.Insecticide resistance in Tephritid flies.Pesticide Biochemistry&Physiology,100(3):199-205.
Wang FY,Yang L,Li LF,Liao SC,Liao RZ,2018.Selection of reference genes in the Bactrocera cucurbitae(Coquillett)under temperature stress by RT-qPCR.Journal of Environmental Entomology,40(5):1097-1105.[王凤英,杨朗,黎柳锋,廖世纯,廖仁昭,姜建军,2018.不同温度胁迫下瓜实蝇RT-qPCR内参基因筛选.环境昆虫学报,40(5):1097-1105.]
Wang HH,Reitz SR,Wang LX,Wang SY,Li X,Lei ZR,2014.The m RNA expression profiles of five heat shock protein genes from Frankliniella occidentalis at different stages and their responses to temperatures and insecticides.Journal of Integrative Agriculture,13(10):2196-2210.
Wang LD,Shan D,Yao J,Fang JC,2015.Induced expression of the heat shock protein 70 and 90 genes by exposure to high temperature and chlorpyrifosin female of Lanodelphax striatellus.Chinese Journal of Applied Entomology,52(4):828-836.[王利华,单丹,姚静,方继朝,2015.温度和毒死蜱对灰飞虱雌成虫热激蛋白70和90基因的诱导表达特性研究.应用昆虫学报,52(4):828-836.]
Wang QX,Li ZY,Xie Y,Cao H,2008.Research progress of heat shock proteins in Drosophila.Chinese Bulletin of Entomology,45(5):698-702.[王秋香,李宗芸,谢艳,曹慧,2008.果蝇热激蛋白的研究进展.昆虫知识,45(5):698-702.]
Wu YK,Zou C,Fu DM,Zhang WN,Xiao HJ,2018.Molecular characterization of three Hsp90 from Pierisand expression patterns in response to cold and thermal stress in summer and winter diapause of Pieris melete.Insect Science,25(2):273-283.
Yang J,Nasir AB,Fan D,2017.cDNA Cloning and induction of heat shock protein Hsp90 from Mythimna separata.Chinese Journal of Biological Control,33(5):623-630.[杨静,Baloch Nasir Ali,樊东,2017.黏虫热休克蛋白Hsp90基因的克隆及不同温度对其诱导反应.中国生物防治学报,33(5):623-630.]
Yang LH,Dou W,Jiang HB,Niu JZ,Ding TB,Wang JJ,2016.Cloning and expression profiling of heat shock protein gene Pc Hsp90 in the citrus red mite,Panonychus citri(Acari:Tetranychidae).Acta Entomologica Sinica,59(4):411-420.[杨丽红,豆威,蒋红波,牛金志,丁天波,王进军,2016.柑橘全爪螨热激蛋白基因Pc Hsp90的克隆及表达模式分析.昆虫学报,59(4):411-420.]
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