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The small heat shock protein Hsp20.8 imparts tolerance to high temperatures in the leafminer fly, Liriomyza trifolii (Diptera: Agtomyzidae)

Published online by Cambridge University Press:  13 March 2024

Yue Zhang ,
Ya-Wen Chang Open the ORCID record for Ya-Wen Chang [Opens in a new window] ,
Yu-Cheng Wang ,
Yu-Qing Yan  and
Yu-Zhou Du Open the ORCID record for Yu-Zhou Du [Opens in a new window]
Yue Zhang
Affiliation:
College of Plant Protection, Yangzhou University, Yangzhou, China
Ya-Wen Chang*
Affiliation:
College of Plant Protection, Yangzhou University, Yangzhou, China
Yu-Cheng Wang
Affiliation:
College of Plant Protection, Yangzhou University, Yangzhou, China
Yu-Qing Yan
Affiliation:
College of Plant Protection, Yangzhou University, Yangzhou, China
Yu-Zhou Du*
Affiliation:
College of Plant Protection, Yangzhou University, Yangzhou, China Joint International Research Laboratory of Agriculture and Agri-Product Safety, The Ministry of Education, Yangzhou University, Yangzhou, China
*
Corresponding author: Ya-Wen Chang; Email: changyawen@yzu.edu.cn
Corresponding author: Ya-Wen Chang; Email: changyawen@yzu.edu.cn
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Abstract

As an environmental factor, temperature impacts the distribution of species and influences interspecific competition. The molecular chaperones encoded by small heat shock proteins (sHsps) are essential for rapid, appropriate responses to environmental stress. This study focuses on Hsp20.8, which encodes a temperature-responsive sHsp in Liriomyza trifolii, an insect pest that infests both agricultural and ornamental crops. Hsp20.8 expression was highest at 39℃ in L. trifolii pupae and adults, and expression levels were greater in pupae than in adults. Recombinant Hsp20.8 was expressed in Escherichia coli and conferred a higher survival rate than the empty vector to bacterial cells exposed to heat stress. RNA interference experiments were conducted using L. trifolii adults and prepupae and the knockdown of Hsp20.8 expression increased mortality in L. trifolii during heat stress. The results expand our understanding of sHsp function in Liriomyza spp. and the ongoing adaptation of this pest to climate change. In addition, this study is also important for predicting the distribution of invasive species and proposing new prevention and control strategies based on temperature adaptation.

Keywords

high-temperature treatmentHsp20.8Liriomyza trifoliiRNA interferencestress response
Type
Research Paper
Information
Bulletin of Entomological Research , First View , pp. 1 - 7
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Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press

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References

Abe, Y and Tokumaru, S (2008) Displacement in two invasive species of leafminer fly in different localities. Biological Invasions 10, 951–953.CrossRefGoogle Scholar
Badillo-Vargas, IE, Rotenberg, D, Schneweis, BA and Whitfield, AE (2015) RNA interference tools for the western flower thrips, Frankliniella occidentalis. Journal of Insect Physiology 76, 36–46.CrossRefGoogle ScholarPubMed
Baneyx, F (1999) Recombinant protein expression in Escherichia coli. Current Opinion in Biotechnology 10, 411–421.CrossRefGoogle ScholarPubMed
Basha, E, O'Neill, H and Vierling, E (2012) Small heat shock proteins and α-crystallins: dynamic proteins with flexible functions. Trends in Biochemical Sciences 37, 106–117.CrossRefGoogle ScholarPubMed
Chang, YW, Chen, JY, Lu, MX, Gao, Y, Tian, ZH, Gong, WR, Dong, CS and Du, YZ (2017a) Cloning and expression of genes encoding heat shock proteins in Liriomyza trifolii and comparison with two congener leafminer species. PLoS ONE 12, e0181355.CrossRefGoogle ScholarPubMed
Chang, YW, Chen, JY, Lu, MX, Gao, Y, Tian, ZH, Gong, WR, Zhu, W and Du, YZ (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, e0181862.CrossRefGoogle ScholarPubMed
Chang, YW, Zhang, XX, Lu, MX, Du, YZ and Zhu-Salzman, K (2019) Molecular cloning and characterization of small heat shock protein genes in the invasive leaf miner fly, Liriomyza trifolii. Genes 10, 775.CrossRefGoogle ScholarPubMed
Chang, YW, Wang, YC, Zhang, XX, Iqbal, J and Du, YZ (2021a) RNA interference of genes encoding the vacuolar-ATPase in Liriomyza trifolii. Insects 12, 41.CrossRefGoogle ScholarPubMed
Chang, YW, Wang, YC, Zhang, XX, Iqbal, J, Lu, MX and Du, YZ (2021b) Transcriptional regulation of small heat shock protein genes by heat shock factor 1 (HSF1) in Liriomyza trifolii under heat stress. Cell Stress and Chaperones 26, 835–843.CrossRefGoogle ScholarPubMed
Chang, YW, Wang, YC, Yan, YQ, Xie, HF, Yuan, DR and Du, YZ (2022) RNA interference of chitin synthase 2 gene in Liriomyza trifolii through immersion in double-stranded RNA. Insects 13, 832.CrossRefGoogle ScholarPubMed
Chen, B and Kang, L (2002) Cold hardiness and supercooling capacity in the pea leafminer Liriomyza huidobrensis. Cryo Letters 23, 173–182.Google ScholarPubMed
Derocher, AE, Helm, KW, Lauzon, LM and Vierling, E (1991) Expression of a conserved family of cytoplasmic low molecular weight heat shock proteins during heat stress and recovery. Plant Physiology 96, 1038–1047.CrossRefGoogle ScholarPubMed
Dong, CL, Zhu, F, Lu, MX and Du, YZ (2021) Characterization and functional analysis of Cshsp19.0 encoding a small heat shock protein in Chilo suppressalis (Walker). International journal of Biological Macromolecules 188, 924–931.CrossRefGoogle ScholarPubMed
Dong, B, Liu, XY, Li, B, Li, MY, Li, SG and Liu, S (2022) A heat shock protein protects against oxidative stress induced by lambda-cyhalothrin in the green peach aphid Myzus persicae. Pesticide Biochemistry and Physiology 181, 104995.CrossRefGoogle ScholarPubMed
Feder, ME and Hofmann, GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annual Review of Physiology 61, 243–282.CrossRefGoogle ScholarPubMed
Franck, E, Madsen, O, van Rheede, T, Ricard, G, Huynen, MA and de Jong, WW (2004) Evolutionary diversity of vertebrate small heat shock proteins. Journal of Molecular Evolution 59, 792–805.CrossRefGoogle ScholarPubMed
Gehring, WJ and 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.CrossRefGoogle ScholarPubMed
Haslbeck, M and Vierling, E (2015) A first line of stress defense: small heat shock proteins and their function in protein homeostasis. Journal of Molecular Biology 427, 1537–1548.CrossRefGoogle ScholarPubMed
Hu, JT, Chen, B and Li, ZH (2014) Thermal plasticity is related to the hardening response of heat shock protein expression in two Bactrocera fruit flies. Journal of Insect Physiology 67, 105–113.CrossRefGoogle Scholar
Huang, LH and 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.CrossRefGoogle ScholarPubMed
Jagla, T, Dubińska-Magiera, M, Poovathumkadavil, P, Daczewska, M and Jagla, K (2018) Developmental expression and functions of the small heat shock proteins in Drosophila. International Journal of Molecular Sciences 19, 3441.CrossRefGoogle ScholarPubMed
Joga, MR, Zotti, MJ, Smagghe, G and Christiaens, O (2016) RNAi efficiency, systemic properties, and novel delivery methods for pest insect control: what we know so far. Frontiers in Physiology 7, 553.CrossRefGoogle ScholarPubMed
Johnson, MW, Welter, SC, Toscano, NC, Ting, P and Trumble, JT (1983) Reduction of tomato leaflet photosynthesis rates by mining activity of Liriomyza sativae (Diptera: Agromyzidae). Journal of Economic Entomology 76, 1061–1063.CrossRefGoogle Scholar
Johnston, JA, Ward, CL and Kopito, RR (1998) Aggresomes: a cellular response to misfolded proteins. The Journal of Cell Biology 143, 1883–1898.CrossRefGoogle ScholarPubMed
Kang, L, Chen, B, Wei, JN and Liu, TX (2009) Roles of thermal adaptation and chemical ecology in Liriomyza distribution and control. Annual Review of Entomology 54, 127–145.CrossRefGoogle ScholarPubMed
King, AM and MacRae, TH (2015) Insect heat shock proteins during stress and diapause. Annual Review of Entomology 60, 59–75.CrossRefGoogle ScholarPubMed
Li, DC, Yang, F, Lu, B, Chen, DF and Yang, WJ (2012) Thermotolerance and molecular chaperone function of the small heat shock protein HSP20 from hyperthermophilic archaeon, Sulfolobus solfataricus P2. Cell Stress and Chaperones 17, 103–108.CrossRefGoogle ScholarPubMed
Liu, Z, Xi, D, Kang, M, Guo, X and Xu, B (2012) Molecular cloning and characterization of Hsp27.6: the first reported small heat shock protein from Apis cerana cerana. Cell Stress and Chaperones 17, 539–551.CrossRefGoogle ScholarPubMed
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402–408.CrossRefGoogle ScholarPubMed
Lu, MX, Hua, J, Cui, YD and Du, YZ (2014) Five small heat shock protein genes from Chilo suppressalis: characteristics of gene, genomic organization, structural analysis, and transcription profiles. Cell Stress and Chaperones 19, 91–104.CrossRefGoogle ScholarPubMed
Morrow, G, Heikkila, JJ and Tanguay, RM (2006) Differences in the chaperone-like activities of the four main small heat shock proteins of Drosophila melanogaster. Cell Stress and Chaperones 11, 51–60.CrossRefGoogle ScholarPubMed
Pacheco, A, Pereira, C, Almeida, MJ and Sousa, MJ (2009) Small heat-shock protein Hsp12 contributes to yeast tolerance to freezing stress. Microbiology 155, 2021–2028.CrossRefGoogle ScholarPubMed
Pan, DD, Lu, MX, Li, QY and Du, YZ (2018) Characteristics and expression of genes encoding two small heat shock protein genes lacking introns from Chilo suppressalis. Cell Stress and Chaperones 23, 55–64.CrossRefGoogle ScholarPubMed
Parrella, MP, Jones, VP, Youngman, RR and Lebeck, LM (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.CrossRefGoogle Scholar
Pérez-Morales, D, Ostoa-Saloma, P and Espinoza, B (2009) Trypanosoma cruzi SHSP16: characterization of an alpha-crystallin small heat shock protein. Experimental Parasitology 123, 182–189.CrossRefGoogle ScholarPubMed
Reitz, SR and Trumble, JT (2002) Interspecific and intraspecific differences in two Liriomyza leafminer species in California. Entomologia Experimentalis et Applicata 102, 101–113.CrossRefGoogle Scholar
Reitz, SR, Kund, GS, Carson, WG, Phillips, PA and Trumble, JT (1999) Economics of reducing insecticide use on celery through low-input pest management strategies. Agriculture Ecosystems and Environment 73, 185–197.CrossRefGoogle Scholar
Spencer, KA (1973) Series Entomologica. In Göttingen, ES (ed.), Agromyzidae (Diptera) of Economic Importance, 1st Edn. Vol. 9. Bath: The Hague Publishers, pp. 19–28.CrossRefGoogle Scholar
Sun, Y and MacRae, TH (2005) Small heat shock proteins: molecular structure and chaperone function. Cellular and Molecular Life Sciences: CMLS 62, 2460–2476.CrossRefGoogle ScholarPubMed
Tabara, H, Grishok, A and Mello, CC (1998) RNAi in C. elegans: soaking in the genome sequence. Science 282, 430–431.CrossRefGoogle Scholar
Tsvetkova, NM, Horváth, I, Török, Z, Wolkers, WF, Balogi, Z, Shigapova, N, Crowe, LM, Tablin, F, Vierling, E, Crowe, JH and Vigh, L (2002) Small heat-shock proteins regulate membrane lipid polymorphism. Proceedings of the National Academy of Sciences of the USA 99, 13504–13509.CrossRefGoogle ScholarPubMed
Wang, ZG, Guan, W and Chen, DH (2007) Preliminary report of the Liriomyza trifolii in Zhongshan area. Plant Quarantine 21, 19–20.Google Scholar
Wang, Y, Zhang, H, Li, H and Miao, X (2011) Second-generation sequencing supply an effective way to screen RNAi targets in large scale for potential application in pest insect control. PLoS ONE 6, e18644.CrossRefGoogle ScholarPubMed
Wang, H, Reitz, SR, Xiang, J, Smagghe, G and Lei, Z (2014a) Does temperature-mediated reproductive success drive the direction of species displacement in two invasive species of leafminer fly? PLoS ONE 9, e98761.CrossRefGoogle ScholarPubMed
Wang, HH, Rreitz, S, Wang, LX, Wang, SY, Xue, LI and Lei, ZR (2014b) 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.CrossRefGoogle Scholar
Wen, JZ, Wang, Y and Lei, ZR (1996) New record of Liriomyza sativae Blanchard (Diptera: Agromyzidae) from China. Entomotaxonomia 18, 311–312.Google Scholar
Wen, JZ, Lei, ZR and Wang, Y (1998) Survey of Liriomyza huidobrensis in Yunnan Province and Guizhou Province, China. Plant Protection 24, 18–20.Google Scholar
Yao, J, Rotenberg, D, Afsharifar, A, Barandoc-Alviar, K and Whitfield, AE (2013) Development of RNAi methods for Peregrinus maidis, the corn planthopper. PLoS ONE 8, e70243.CrossRefGoogle ScholarPubMed
Yu, N, Christiaens, O, Liu, J, Niu, J, Cappelle, K, Caccia, S, Huvenne, H and Smagghe, G (2013) Delivery of dsRNA for RNAi in insects: an overview and future directions. Insect Science 20, 4–14.CrossRefGoogle ScholarPubMed
Yuan, JW, Song, HX, Chang, YW, Yang, F, Xie, HF, Gong, WR and Du, YZ (2022) Identification, expression analysis and functional verification of two genes encoding small heat shock proteins in the western flower thrips, Frankliniella occidentalis (Pergande). International Journal of Biological Macromolecules 211, 74–84.CrossRefGoogle ScholarPubMed
Zhang, Y, Liu, Y, Guo, X, Li, Y, Gao, H, Guo, X and Xu, B (2014) sHsp22.6, an intronless small heat shock protein gene, is involved in stress defence and development in Apis cerana cerana. Insect Biochemistry and Molecular Biology 53, 1–12.CrossRefGoogle ScholarPubMed
Zhang, H, Li, H, Guan, R and Miao, X (2015) Lepidopteran insect species-specific, broad-spectrum, and systemic RNA interference by spraying dsRNA on larvae. Entomologia Experimentalis et Applicata 155, 218–228.CrossRefGoogle Scholar
Zhao, L and Jones, WA (2012) Expression of heat shock protein genes in insect stress responses. Invertebrate Survival Journal 9, 93–101.Google Scholar