Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-27T05:42:52.242Z Has data issue: false hasContentIssue false
  • English
  • Français

Characterization of three heat shock protein 70 genes from Liriomyza trifolii and expression during thermal stress and insect development

Published online by Cambridge University Press:  10 May 2018

Y.-W. Chang ,
X.-X. Zhang ,
J.-Y. Chen ,
M.-X. Lu ,
W.-R. Gong  and
Y.-Z. Du
Y.-W. Chang
Affiliation:
School of Horticulture and Plant Protection & Institute of Applied Entomology, Yangzhou University, Yangzhou 225009, China
X.-X. Zhang
Affiliation:
School of Horticulture and Plant Protection & Institute of Applied Entomology, Yangzhou University, Yangzhou 225009, China
J.-Y. Chen
Affiliation:
School of Horticulture and Plant Protection & Institute of Applied Entomology, Yangzhou University, Yangzhou 225009, China Laboratory for Prevention and Control of Alien Pests, Suzhou Entry-Exit Inspection and Quarantine Bureau, Suzhou 215000, China
M.-X. Lu
Affiliation:
School of Horticulture and Plant Protection & Institute of Applied Entomology, Yangzhou University, Yangzhou 225009, China
W.-R. Gong
Affiliation:
Plant Protection and Quarantine Station of Jiangsu Province, Nanjing 21003, China
Y.-Z. Du*
Affiliation:
School of Horticulture and Plant Protection & Institute of Applied Entomology, Yangzhou University, Yangzhou 225009, China Joint International Research Laboratory of Agriculture and Agri-Product Safety, the Ministry of Education, Yangzhou University, Yangzhou 25009, China
*
*Author for correspondence Phone: 086-514-87971854 Fax: 086-514-87347537 E-mail: yzdu@yzu.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Heat shock proteins (HSPs) participate in diverse physiological processes in insects, and HSP70 is one of the most highly conserved proteins in the HSP family. In this study, full-length cDNAs of three HSP70 genes (Lthsc70, Lthsp701, and Lthsp702) were cloned and characterized from Liriomyza trifolii, an important invasive pest of vegetable crops and horticultural crops worldwide. These three HSP70s exhibited signature sequences and motifs that are typical of the HSP70 family. The expression patterns of the three Lthsp70s during temperature stress and in different insect development stages were studied by real-time quantitative PCR. Lthsp701 was strongly induced by high- and low-temperature stress, but Lthsc70 and Lthsp702 were not very sensitive to temperature changes. All three Lthsp70s were expressed during insect development stages, but the expression patterns were quite different. The expression of Lthsc70 and Lthsp702 showed significant differences in expression during leafminer development; Lthsc70 was most highly expressed in female adults, whereas Lthsp702 was abundantly expressed in larvae and prepupae. Lthsp701 expression was not significantly different among leafminer stages. These results suggest that functional differentiation within the LtHSP70 subfamily has occurred in response to thermal stress and insect development.

Keywords

Liriomyza trifoliiheat shock protein 70thermal stressdevelopmental stageexpression profile
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 109 , Issue 2 , April 2019 , pp. 150 - 159
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abe, Y. & Kawahara, T. (2001) Coexistence of the vegetable leafminer, Liriomyza sativae (Diptera: Agromyzidae), with L. trifolii and L. bryoniae on commercially grown tomato plants. Applied Entomology and Zoology 36, 277–281.Google Scholar
Abe, Y. & Tokumaru, S. (2008) Displacement in two invasive species of leafminer fly in different localities. Biological Invasions 10, 951–953.Google Scholar
Bale, J.S. (2002) Insects and low temperatures: from molecular biology to distributions and abundance. Philosophical Transactions of the Royal Society B: Biological Sciences 357, 849–862.Google Scholar
Bale, J.S., Masters, G.J., Hodkinson, I.D., Awmack, C., Bezemer, T.M., Brown, V.K., Butterfield, J., Buse, A., Coulson, J.C., Farrar, J., Good, J.E.G., Harrington, R., Hartley, S., Jones, T.H., Lindroth, R.L., Press, M.C., Symrnioudis, I., Watt, A.D. & Whittaker, J.B. (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biology 8, 1–16.Google Scholar
Bettencourt, B.R., Hogan, C.C., Nimali, M. & Drohan, B.W. (2008) Inducible and constitutive heat shock gene expression responds to modification of Hsp70 copy number in Drosophila melanogaster but does not compensate for loss of thermotolerance in Hsp70 null flies. BMC Biology 6, 5.Google Scholar
Boorstein, W.R., Ziegelhoffer, T. & Craig, E.A. (1994) Molecular evolution of the HSP70 multigene family. Journal of Molecular Evolution 38, 1–17.Google Scholar
Burton, V., Mitchell, H.K., Young, P. & Petersen, N.S. (1988) Heat shock protection against cold stress of Drosophila melanogaster. Molecular and Cellular Biology 8, 3550–3552.Google Scholar
Castillo-Davis, C.I., Mekhedov, S.L., Hartl, D.L., Koonin, E.V. & Kondrashov, F.A. (2002) Selection for short introns in highly expressed genes. Nature Genetics 31, 415–418.Google Scholar
Chang, Y.W., Chen, J.Y., Lu, M.X., Gao, Y., Tian, Z.H., Gong, W.R., Dong, C.S. & Du, Y.Z. (2017a) Cloning and expression of genes encoding heat shock proteins in Liriomyza trifolii and comparison with two congener leafminer species. PLoS ONE 12(7), e0181355.Google Scholar
Chang, Y.W., Chen, J.Y., Lu, M.X., Gao, Y., Tian, Z.H., Gong, W.R., Zhu, W. & Du, Y.Z. (2017b) Selection and validation of reference genes for quantitative real-time PCR analysis under different experimental conditions in the leafminer Liriomyza trifolii (Diptera: Agromyzidae). PLoS ONE 12(7), e0181862.Google Scholar
Chen, B. & Kang, L. (2002) Cold hardiness and supercooling capacity in the pea leafminer Liriomyza huidobrensis. CryoLetters 23, 173–182.Google Scholar
Cheng, W., Li, D., Wang, Y., Liu, Y. & Zhu-Salzman, K. (2016) Cloning of heat shock protein genes (hsp70, hsc70 and hsp90) and their expression in response to larval diapause and thermal stress in the wheat blossom midge, Sitodiplosis mosellana. Journal of Insect Physiology 95, 66–77.Google Scholar
Chidawanyika, F. & Terblanche, J.S. (2011) Rapid thermal responses and thermal tolerance in adult codling moth Cydia pomonella (Lepidoptera: Tortricidae). Journal of Insect Physiology 57, 108–117.Google Scholar
Comeron, J.M. (2004) Selective and mutational patterns associated with gene expression in humans influences on synonymous composition and intron presence. Genetics 167, 1293–1304.Google Scholar
Cui, Y.D., Lu, M.X. & Du, Y.Z. (2010) Cloning of the heat shock protein 70 gene from Chilo suppressalis and the analysis of its expression characteristics under heat stress. Acta Entomologica Sinica 53, 841–848.Google Scholar
Daugaard, M., Rohde, M. & Jäättelä, M. (2007) The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Letters 581, 3702–3710.Google Scholar
Denlinger, D.L. (2002) Regulation of diapause. Annual Review of Entomology 47, 93–122.Google Scholar
Duman, J.G. (2003) Antifreeze and ice nucleator proteins in terrestrial arthropods. Annual Review of Physiology 63, 327–357.Google Scholar
Feder, M.E. & Hofmann, G.E. (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annual Review of Physiology 61, 243–282.Google Scholar
Flaherty, K.M., Deluca-Flaherty, C. & Mckay, D.B. (1990) Three dimensional structures of the ATPase fragment of a 70 kDa heat shock protein. Nature 346, 623–628.Google Scholar
Flaherty, K.M., Wilbanks, S.M., Deluca-Flaherty, C. & Mckay, D.B. (1994) Structural basis of the 70-kilodalton heat shock cognate protein ATP hydrolytic activity. II. Structure of the active site with ADP or ATP bound to wild type and mutant ATPase fragment. Journal of Biological Chemistry 269, 12899–12907.Google Scholar
Fung, K.L., Hilgenberg, L., Wang, N.M. & Chirico, W.J. (1996) Conformations of the nucleotide and polypeptide binding domains of a cytosolic Hsp70 molecular chaperone are coupled. Journal of Biological Chemistry 271, 21559–21565.Google Scholar
Gao, Y.L. & Reitz, S.R. (2016) Emerging themes in our understanding of species displacements. Annual Review of Entomology 62, 163–183.Google Scholar
Gao, Y.L., Reitz, S., Xing, Z.L., Ferguson, S. & Lei, Z.R. (2017) A decade of a leafminer invasion in China: lessons learned. Pest Management Science 73, 1775–1779.Google Scholar
Gehring, W.J. & Wehner, R. (1995) Heat shock protein synthesis and thermotolerance in Cataglyphis, an ant from the Sahara desert. Proceedings of the National Academy of Sciences of the USA 92, 2994–2998.Google Scholar
Grace, M.L., Chandrasekharan, M.B., Hall, T.C. & Crowe, A.J. (2004) Sequence and spacing of TATA box elements are critical for accurate initiation from the beta-phaseolin promoter. Journal of Biological Chemistry 279, 8102–8110.Google Scholar
Gupta, R.S. & Singh, B. (1994) Phylogenetic analysis of 70 kd heat shock protein sequences suggests a chimeric origin for the eukaryotic cell nucleus. Current Biology 4, 1104–1114.Google Scholar
Haass, C., Klein, U. & Kloetzel, P.M. (1990) Developmental expression of Drosophila melanogaster small heat-shock proteins. Journal of Cell Science 96, 413–418.Google Scholar
Hoffmann, A.A., Sørensen, J.G. & Loeschcke, V. (2003) Adaptation of Drosophila, to temperature extremes: bringing together quantitative and molecular approaches. Journal of Thermal Biology 28, 175–216.Google Scholar
Huang, L.H. & Kang, L. (2007) Cloning and interspecific altered expression of heat shock protein genes in two leafminer species in response to thermal stress. Insect Molecular Biology 16, 491–500.Google Scholar
Huang, L.H., Chen, B. & Kang, L. (2007) Impact of mild temperature hardening on thermotolerance, fecundity, and Hsp gene expression in Liriomyza huidobrensis. Journal of Insect Physiology 53, 1199–1205.Google Scholar
Huang, L.H., Wang, C.Z. & Kang, L. (2009) Cloning and expression of five heat shock protein genes in relation to cold hardening and development in the leafminer, Liriomyza sativa. Journal of Insect Physiology 55, 279–285.Google Scholar
Hunt, C & Morimoto, R.I. (1985) Conserved features of eukaryotic hsp70 genes revealed by comparison with the nucleotide sequence of Human hsp70. Proceedings of the National Academy of Sciences of the USA 82, 6455–6459.Google Scholar
Ji, Q.Z., Wang, H.H., Lei, Z.R., Zhang, K.W., Wang, J. & Zhang, Y. (2013) Cloning and expression of heat shock protein 90 gene in relation to heat stress in the leafminer, Liriomyza trifolii. Plant Protection 39, 110–116.Google Scholar
Johnson, M.W., Welter, S.C., Toscano, N.C., Tingi, P. & Trumble, J.T. (1983) Reduction of tomato leaflet photosynthesis rates by mining activity of Liriomyza sativae (Diptera: Agromyzidae). Journal of Economic Entomology 76, 1061–1063.Google Scholar
Johnston, J.A., Ward, C.L. & Kopito, R.R. (1998) Aggresomes: a cellular response to misfolded proteins. Journal of Cell Biology 143, 1883–1898.Google Scholar
Joplin, K.H. & Denlinger, D.L. (1990) Developmental and tissue specific control of the heat shock induced 70 kDa related proteins in the flesh fly, Sarcophaga crassipalpis. Journal of Insect Physiology 36, 239–249.Google Scholar
Kang, L., Chen, B., Wei, J.N. & Liu, T.X. (2009) Roles of thermal adaptation and chemical ecology in Liriomyza distribution and control. Annual Review of Entomology 54, 127–145.Google Scholar
Karlin, S. & Brocchieri, L. (1998) Heat shock protein 70 family: multiple sequence comparisons, function, and evolution. Journal of Molecular Evolution 47, 565–577.Google Scholar
Kelly, S.A., Panhuis, T.M. & Stoehr, A.M. (2012) Phenotypic plasticity: molecular mechanisms and adaptive significance. Comprehensive Physiology 2, 1417–1439.Google Scholar
Kiang, J.G. & Tsokos, G.C. (1998) Heat shock protein 70 kDa: molecular biology, biochemistry, and physiology. Pharmacology & Therapeutics 80, 183–201.Google Scholar
Knowlton, A.A. & Salfity, M. (1996) Nuclear localization and the heat shock proteins. Journal of Biosciences 21, 123–132.Google Scholar
Lei, Z.R., Yao, J.M., Zhu, C.J. & Wang, H.H. (2007) Prediction of suitable areas for Liriomyza trifolii (Burgess) in China. Plant Protection 33, 100–103.Google Scholar
Lezzi, M. (1996) Chromosome puffing: supramolecular aspects of ecdysone action. pp. 145–173 in Gilbert, L.I., Tata, J.R. & Atkinson, B.G. (Eds) Metamorphosis: Post-Embryonic Reprogramming of Gene Expression in Amphibian and Insect Cells. New York, Academic Press.Google Scholar
Li, A.Q., Popovabutler, A., Dean, D.H. & Denlinger, D.L. (2007) Proteomics of the flesh fly brain reveals an abundance of upregulated heat shock proteins during pupal diapause. Journal of Insect Physiology 53, 385–391.Google Scholar
Lindquist, S. & Craig, E.A. (1988) The heat-shock proteins. Annual Review of Genetics 22, 631–677.Google Scholar
Livak, K.J. & Schmittgen, T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402–408.Google Scholar
Lu, M.X., Hua, J., Cui, Y.D. & Du, Y.Z. (2014) Five small heat shock protein genes from Chilo suppressalis: characteristics of gene, genomic organization, structural analysis, and transcription profiles. Cell Stress & Chaperones 19, 91–104.Google Scholar
Lu, M.X., Li, H.B., Zheng, Y.T., Shi, L. & Du, Y.Z. (2016) Identification, genomic organization and expression profiles of four heat shock protein genes in the western flower thrips, Frankliniella occidentalis. Journal of Thermal Biology 57, 110–118.Google Scholar
Lü, Z.C., Wang, Y.M., Zhu, S.G., Yu, H., Guo, J.Y. & Wan, F.H. (2014) Trade-offs between survival, longevity, and reproduction, and variation of survival tolerance in Mediterranean Bemisia tabaci after temperature stress. Journal of Insect Science 14, 124.Google Scholar
Macrae, T.H. (2010) Gene expression, metabolic regulation and stress tolerance during diapause. Cellular and Molecular Life Sciences 67, 2405–2424.Google Scholar
Mahroof, R., Yan, Z.K., Neven, L., Subramanyam, B. & Bai, J. (2005) Expression patterns of three heat shock protein 70 genes among developmental stages of the red flour beetle, Tribolium castaneum (Coleoptera: Tenebrionidae). Comparative Biochemistry and Physiology – Part A: Molecular & Integrative Physiology 141, 247–256.Google Scholar
Mayer, M.P. & Bukau, B. (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cellular and Molecular Life Sciences 62, 670–684.Google Scholar
Mcdonald, J.R., Bale, J.S., Walters, K.F.A., Bale, J.S., Block, W. & Sømme, L. (1999) Temperature, development and establishment potential of Thrips palmi (Thysanoptera: Thripidae) in the United Kingdom. European Journal of Entomology 96, 169–173.Google Scholar
Mclaughlin, S.H., Sobott, F., Yao, Z.P., Zhang, W., Nielsen, P.R., Grossmann, J.G., Laue, E.D., Robinson, C.V. & Jackson, SE. (2006) The co-chaperone p23 arrests the Hsp90 ATPase cycle to trap client proteins. Journal of Molecular Biology 356, 746–758.Google Scholar
Morano, K.A., Sistonen, L. & Mezger, V. (2014) Heat shock in the springtime. Cell Stress & Chaperones 19, 753–761.Google Scholar
Moseley, P.L. (1997) Heat shock proteins and heat adaptation of the whole organism. Journal of Applied Physiology 83, 1413–1417.Google Scholar
Mount, S.M. (1982) A catalog of splice junction sequences. Nucleic Acids Research 10, 459–472.Google Scholar
Parrella, M.P., Jones, V.P., Youngman, R.R. & Lebeck, L.M. (1985) Effect of leaf mining and leaf stippling of Liriomyza spp. on photosynthetic rates of chrysanthemum. Annals of the Entomological Society of America 78, 90–93.Google Scholar
Parsell, D.A. & Lindquist, S. (1993) The function of heat-shock proteins in stress tolerance: degradation and reactivation of damaged proteins. Annual Review of Genetics 27, 437–496.Google Scholar
Parsell, D.A., Taulien, J. & Lindquist, S. (1993) The role of heat-shock proteins in thermotolerance. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 339, 279–285.Google Scholar
Pockley, A., Muthanal, M. & Calderwood, S. (2008) The dual immunoregulatory roles of stress proteins. Trends in Biochemical Sciences 33, 71–79.Google Scholar
Qiao, L., Wu, J.X., Qin, D.Z., Liu, X.C., Lu, Z.C., Lv, L.Z., Pan, Z.L., Chen, H. & Li, G.W. (2015) Gene expression profiles of heat shock proteins 70 and 90 from Empoasca onukii (Hemiptera: Cicadellidae) in response to temperature stress. Journal of Insect Science 15, 49.Google Scholar
Reitz, S.R. & Trumble, J.T. (2002a) Interspecific and intraspecific differences in two Liriomyza leafminer species in California. Entomologia Experimentalis et Applicata 102, 101–113.Google Scholar
Reitz, S.R. & Trumble, J.T. (2002b) Competitive displacement among insects and arachnids. Annual Review of Entomology 47, 435–465.Google Scholar
Reitz, S.R., Kund, G.S., Carson, W.G., Phillips, P.A. & Trumble, J.T. (1999) Economics of reducing insecticide use on celery through low-input pest management strategies. Agriculture, Ecosystems & Environment 73, 185–197.Google Scholar
Renner, T. & Waters, E.R. (2006) Comparative genomic analysis of the Hsp70s from five diverse photosynthetic eukaryotes. Cell Stress & Chaperones 12, 172–185.Google Scholar
Rinehart, J.P., Yocum, G.D. & Denlinger, D.L. (2000) Developmental upregulation of inducible hsp70 transcripts, but not the cognate form, during pupal diapause in the flesh fly, Ssarcophaga crassipalpis. Insect Biochemistry and Molecular Biology 30, 515–521.Google Scholar
Rinehart, J.P., Li, A., Yocum, G.D., Robich, R.M., Hayward, S.A. & Denlinger, DL. (2007) Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proceedings of the National Academy of Sciences of the USA 104, 11130–11137.Google Scholar
Ryan, J.A. & Hightower, L.E. (1998) Heat shock proteins: molecular biomarkers of effects. pp. 449–466 in Puga, A. & Wallale, K.B. (Eds) Molecular Biology of the Toxic Response. Hamilton Printing Co. New York, Castleton.Google Scholar
Saraste, M., Sibbald, P.R. & Wittinghofer, A. (1990) The P-loop-a common motif in ATP- and GTP-binding proteins. Trends in Biochemical Sciences 15, 430–434.Google Scholar
Shen, Q.D., Zhao, L., Xie, G.Q., Wei, P., Yang, M.M., Wang, S.G., Zhang, F. & Tang, B. (2015) Cloning three Harmonia axyridis (Coleoptera: Coccinellidae) heat shock protein 70 family genes: regulatory function related to heat and starvation stress. Journal of Entomological Science 50, 168–185.Google Scholar
Shim, J.K., Jung, D.O., Park, J.W., Kim, D.W., Ha, D.M. & Lee, K.Y. (2006) Molecular cloning of the heat-shock cognate 70 (Hsc70) gene from the two-spotted spider mite, Tetranychus urticae, and its expression in response to heat shock and starvation. Comparative Biochemistry and Physiology – Part A: Molecular & Integrative Physiology 145, 288–295.Google Scholar
Siligardi, G., Hu, B., Panaretou, B., Piper, P.W., Pearl, L.H. & Prodromou, C. (2005) Co-chaperone regulation of conformational switching in the Hsp90 ATPase cycle. Journal of Biological Chemistry 279, 51989–51998.Google Scholar
Sonoda, S., Ashfaq, M. & Tsumuki, H. (2006) Cloning and nucleotide sequencing of three heat shock protein genes (hsp90, hsc70, and hsp19.5) from the diamondback moth, Plutella xylostella (L.) and their expression in relation to developmental stage and temperature. Archives of Insect Biochemistry and Physiology 62, 80–90.Google Scholar
Sørensen, J.G., Kristensen, T.N. & Loeschcke, V. (2003) The evolutionary and ecological role of heat shock proteins. Ecology Letters 6, 1025–1037.Google Scholar
Spencer, K.A. (1973) Agromyzidae (Diptera) of economic importance. pp. 19–28 in Schimitschek, E. & Göttingen, (Eds) Series Entomologica (Vol. 9). Bath, UK, The Pitman Press.Google Scholar
Sun, Y., Zhao, J., Sheng, Y., Xiao, Y.F., Zhang, Y.J., Bai, L.X., Tan, Y.G., Xiao, L.B. & Xu, G.C. (2016) Identification of heat shock cognate protein 70 gene (Alhsc70) of Apolygus lucorum and its expression in response to different temperature and pesticide stresses. Insect Science 23, 37–49.Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.Google Scholar
Tang, T., Wu, C., Li, J., Ren, G., Huang, D. & Liu, F. (2012) Stress-induced hsp70 from Musca domestica plays a functionally significant role in the immune system. Journal of Insect Physiology 58, 1226–1234.Google Scholar
Taylor, F. (1981) Ecology and evolution of physiological time in insects. American Naturalist 117, 1–23.Google Scholar
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The Clustal-x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.Google Scholar
Tissières, A., Mitchell, H.K. & Tracy, U.M. (1974) Protein synthesis in salivary glands of Drosophila melanogaster: relation to chromosome puffs. Journal of Molecular Biology 84, 389–398.Google Scholar
Velazquez, J.M. & Lindquist, S. (1984) Hsp70: nuclear concentration during environmental stress and cytoplasmic storage during recovery. Cell 36, 655–662.Google Scholar
Wang, H., Dong, S.Z., Li, K., Hu, C. & Ye, G.Y. (2008) A heat shock cognate 70 gene in the endoparasitoid, Pteromalus puparum, and its expression in relation to thermal stress. BMB Reports 41, 388–393.Google Scholar
Wang, H.H., Rreitz, S., Wang, L.X., Wang, S.Y., Xue, L.I. & Lei, Z.R. (2014) The mRNA 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, 2196–2210.Google Scholar
Wang, Z.G., Guan, W. & Chen, D.H. (2007) Preliminary report of the Liriomyza trifolii in Zhongshan area. Plant Quarantine 21, 19–20.Google Scholar
Wen, J.Z., Wang, Y. & Lei, Z.R. (1996) New record of Liriomyza sativae Blanchard (Diptera: Agromyzidae) from China. Entomotaxonomia 18, 311–312.Google Scholar
Wen, J.Z., Lei, Z.R. & Wang, Y. (1998) Survey of Liriomyza huidobrensis in Yunnan Province and Guizhou Province, China. Plant Protection 24, 18–20.Google Scholar
Wu, C.H., Madabusi, L., Nishioka, H., Emanuel, P., Sypes, M., Arkhipova, I. & Gilmour, D.S. (2001) Analysis of core promoter sequences located downstream from the TATA element in the hsp70 promoter from Drosophila melanogaster. Molecular and Cellular Biology 21, 1593–1602.Google Scholar
Xiang, J.C., Lei, Z.R. & Wang, H.H. (2012) Interspecific competition among three invasive Liriomyza species. Acta Ecologica Sinica 32, 1616–1622.Google Scholar
Xiao, H.J., Wei, Z.J. & Xue, F.S. (2011) Progress in heat shock proteins (Hsps) related to insect diapause. Acta Ecologica Sinica 54, 1068–1075.Google Scholar
Xu, P.J., Xiao, J.H., Li, L., Tong, L. & Huang, D.W. (2010) Molecular cloning and characterization of four heat shock protein genes from Macrocentrus cingulum (Hymenoptera: Braconidae). Molecular Biology Reports 37, 2265–2272.Google Scholar
Zhang, L.J., Wang, K.F., Jing, Y.P., Zhuang, H.M. & Wu, G. (2015) Identification of heat shock protein genes hsp70s and hsc70 and their associated mRNA expression under heat stress in insecticide-resistant and susceptible diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). European Journal of Entomology 112, 215–226.Google Scholar
Zhang, Q. & Denlinger, D.L. (2010) Molecular characterization of heat shock protein 90, 70 and 70 cognate cDNAs and their expression patterns during thermal stress and pupal diapause in the corn earworm. Journal of Insect Physiology 56, 138–150.Google Scholar
Zheng, D., Cui, X.H., Li, H.L., Cai, C., Gao, Y.S. & Shang, H.W. (2010) Cloning of heat shock protein gene, hsp70, in Liriomyza trifolii and its expression under temperature stress. Acta Phytophylacica Sinica 37, 159–164.Google Scholar
Zhou, Z.S., Guo, J.Y., Chen, H.S. & Wan, F.H. (2010) Effects of temperature on survival, development, longevity, and fecundity of Ophraella communa (Coleoptera: Chrysomelidae), a potential biological control agent against Ambrosia artemisiifolia (Asterales: Asteraceae). Environmental Entomology 39, 1021–1027.Google Scholar
Supplementary material: File

Chang et al. supplementary material

Figure S1

Download Chang et al. supplementary material(File)
File 1.4 MB
Supplementary material: File

Chang et al. supplementary material

Table S1

Download Chang et al. supplementary material(File)
File 17.2 KB