Abstract
Small heat shock proteins (sHSPs) function as molecular chaperones in multiple physiological processes and are active during thermal stress. sHSP expression is controlled by heat shock transcription factor (HSF); however, few studies have been conducted on HSF in agricultural pests. Liriomyza trifolii is an introduced insect pest of horticultural and vegetable crops in China. In this study, the master regulator, HSF1, was cloned and characterized from L. trifolii, and the expression levels of HSF1 and five sHSPs were studied during heat stress. HSF1 expression in L. trifolii generally decreased with rising temperatures, whereas expression of the five sHSPs showed an increasing trend that correlated with elevated temperatures. All five sHSPs and HSF1 showed an upward trend in expression with exposure to 40 ℃ without a recovery period. When a recovery period was incorporated after thermal stress, the expression patterns of HSF1 and sHSPs in L. trifolii exposed to 40 °C was significantly lower than expression with no recovery period. To elucidate potential interactions between HSF1 and sHSPs, double-stranded RNA was synthesized to knock down HSF1 in L. trifolii by RNA interference. The knockdown of HSF1 by RNAi decreased the survival rate and expression of HSP19.5, HSP20.8, and HSP21.3 during high-temperature stress. This study expands our understanding of HSF1-regulated gene expression in L. trifolii exposed to heat stress.
Similar content being viewed by others
References
Abe Y, Tokumaru S (2008) Displacement in two invasive species of leafminer fly in different localities. Biol Invasions 10:951–953
Åkerfelt M, Morimoto RI, Sistonen L (2010) Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol 8:545–555
Amin J, Ananthan J, Voellmy R (1988) Key features of heat shock regulatory elements. Mol Cell Biol 8:3761–3769
Anckar J, Sistonen L (2007) Heat shock factor 1 as a coordinator of stress and developmental pathways. Adv Exp Med Biol 594:78–88
Anckar J, Sistonen L (2011) Regulation of HSF1 function in the heat shock response: implications in aging and disease. Annu Rev Biochem 80:1089–1115
Brunquell J, Morris S, Lu Y, Cheng F, Westerheide SD (2016) The genome-wide role of HSF-1 in the regulation of gene expression in Caenorhabditis elegans. BMC Genomics 17:559
Chang YW, Chen JY, Lu MX, Gao Y, Tian ZH, Gong WR, Dong CS, Du YZ (2017) Cloning and expression of genes encoding heat shock proteins in Liriomyza trifolii and comparison with two congener leafminer species. PLoS ONE 12:e0181355
Chang YW, Chen JY, Lu MX, Gao Y, Tian ZH, Gong WR, Zhu W, Du YZ (2017) 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
Chang YW, Zhang XX, Lu MX, Du YZ, 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
Chang YW, Wang YC, Zhang XX, Iqbal J, Lu MX, Gong HX, Du YZ (2020a) Comparative transcriptome analysis of three invasive leafminer flies provides insights into interspecific competition. Int J Biol Macromol 165:1664–1674
Chang YW, Zhang XX, Lu MX, Gong WR, Du YZ (2020) Transcriptome analysis of Liriomyza trifolii (Diptera: Agromyzidae) in response to temperature stress. Comp Biochem Phys D 34:100677
Chen B, Kang L (2002) Cold hardiness and supercooling capacity in the pea leafminer Liriomyza huidobrensis. Cryo Lett 23:173–182
Colinet H, Lee SF, Hoffmann A (2010) Temporal expression of heat shock genes during cold stress and recovery from chill coma in adult Drosophila melanogaster. Febs J 277:174–185
Dou W, Tian Y, Liu H, Shi Y, Smagghe G, Wang JJ (2017) Characteristics of six small heat shock protein genes from Bactrocera dorsalis: diverse expression under conditions of thermal stress and normal growth. Comp Biochem Physiol B Biochem Mol Biol 213:8–16
Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282
Franck E, Madsen O, Van-Rheede T, Ricard G, Huynen MA, De-Jong WW (2004) Evolutionary diversity of vertebrate small heat shock proteins. J Mol Evol 59:792–805
Fujikake N, Nagai Y, Popiel HA, Kano H, Yamaguchi M, Toda T (2005) Alternative splicing regulates the transcriptional activity of Drosophila heat shock transcription factor in response to heat/cold stress. FEBS Lett 17:3842–3848
Fujimoto M, Nakai A (2010) The heat shock factor family and adaptation to proteotoxic stress. FEBS J 277:4112–4125
Gao YL, Reitz SR, Xing ZL, Ferguson S, Lei ZR (2017) A decade of a leafminer invasion in China: lessons learned. Pest Manag Sci 73:1775–1779
Gehring WJ, Wehner R (1995) Heat shock protein synthesis and thermotolerance in Cataglyphis, an ant from the Sahara Desert. Proc Natl Acad Sci U S A 92:2994–2998
Gomez-Pastor R, Burchfiel ET, Thiele DJ (2018) Regulation of heat shock transcription factors and their roles in physiology and disease. Nat Rev Mol Cell Biol 19:4–20
Guertin MJ, Petesch SJ, Zobeck KL, Min IM, Lis JT (2010) Drosophila heat shock system as a general model to investigate transcriptional regulation. Cold Spring Harb Symp Quant Biol 75:1–9
Hu JT, Chen B, Li ZH (2014) Thermal plasticity is related to the hardening response of heat shock protein expression in two Bactrocera fruit flies. J Insect Physiol 67:105–113
Huang LH, Kang L (2007) Cloning and interspecific altered expression of heat shock protein genes in two leafminer species in response to thermal stress, Insect Mol. Biol 16:491–500
Jin JS, Li YZ, Zhou ZS, Zhang H, Guo JY, Wan FH (2020) Heat shock factor is involved in regulating the transcriptional expression of two potential hsps (AhHsp70 and AhsHsp21) and its role in heat shock response of Agasicles hygrophila. Front Physiol 11:562204
Johnson MW, Welter SC, Toscano NC, Tingi P, Trumble JT (1983) Reduction of tomato leaflet photosynthesis rates by mining activity of Liriomyza sativae (Diptera: Agromyzidae). J Econ Entomol 76:1061–1063
Johnston JA, Ward CL, Kopito RR (1998) Aggresomes: a cellular response to misfolded proteins. J Cell Biol 143:1883–1898
Kang L, Chen B, Wei JN, Liu TX (2009) Roles of thermal adaptation and chemical ecology in Liriomyza distribution and control. Annu Rev Entomol 54:127–145
Kimpel JA, Nagao RT, Goekjian V, Key JL (1990) Regulation of the heat shock response in soybean seedlings. Plant Physiol 94:988–995
Kovács D, Sigmond T, Hotzi B, Bohár B, Fazekas D, Deák V, Vellai T, Barna J (2019) Hsf1base: a comprehensive database of hsf1 (heat shock factor 1) target genes. Int J Mol Sci 20:5815
Li J, Labbadia J, Morimoto RI (2017) Rethinking HSF1 in stress, development, and organismal health. Trends Cell Biol 27:895–905
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−ΔΔC(T)) method. Methods 25:402–408
Lu MX, Hua J, Cui YD, Du YZ (2014) Five small heat shock protein genes from Chilo suppressalis: characteristics of gene, genomic organization, structural analysis, and transcription profiles. Cell Stress Chaperon 19:91–104
Mahat DB, Salamanca HH, Duarte FM, Danko CG, Lis JT (2016) Mammalian heat shock response and mechanisms underlying its genome-wide transcriptional regulation. Mol Cell 62:63–78
Neef DW, Jaeger AM, Thiele DJ (2011) Heat shock transcription factor 1 as a therapeutic target in neurodegenerative diseases. Nat Rev Drug Discov 10:930–944
Neudegger T, Verghese J, Hayer-Hartl M, Hartl FU, Bracher A (2016) Structure of human heat-shock transcription factor 1 in complex with DNA. Nat Struct Mol Biol 1:140–146
Nielsen MM, Overgaard J, Sørensen JG, Holmstrup M, Justesen J, Loeschcke V (2005) Role of HSF activation for resistance to heat, cold and high-temperature knock-down. J Insect Physiol 51:1320–1329
Pan DD, Lu MX, Li QY, Du YZ (2017) Characteristics and expression of genes encoding two small heat shock protein genes lacking introns from Chilo suppressalis. Cell Stress Chaperon 23:1–10
Parrella MP, Jones VP, Youngman RR, Lebeck LM (1985) Effect of leaf mining and leaf stippling of Liriomyza spp. on photosynthetic rates of chrysanthemum. Ann Entomol Soc A 78:90–93
Quan GX, Duan J, Ladd T, Krell PJ (2017) Identification and expression analysis of multiple small heat shock protein genes in spruce budworm, Choristoneura fumiferana, (l.). Cell Stress Chaperon 23:141–154
Reitz SR, Trumble JT (2002) Interspecific and intraspecific differences in two Liriomyza leafminer species in California. Entomol Exp Appl 102:101–113
Reitz SR, Kund GS, Carson WG, Phillips PA, Trumble JT (1999) Economics of reducing insecticide use on celery through low-input pest management strategies. Agric Ecosyst Environ 73:185–197
Shamovsky I, Nudler E (2008) New insights into the mechanism of heat shock response activation. Cell Mol Life Sci 65:855–861
Spencer KA (1973) Agromyzidae (Diptera) of economic importance. 9: Series Entomologica. The Hague Publishers, Bath, pp 19–28
Steurer C, Eder N, Kerschbaum S, Wegrostek C, Gabriel S, Pardo N, Ortner V, Czerny T, Riegel E (2018) Hsf1 mediated stress response of heavy metals. PLoS ONE 13:e0209077
Takii R, Fujimoto M, Matsuura Y, Wu F, Oshibe N, Takaki E, Katiyar A, Akashi H, Makino T, Kawata M, Naka A (2017) HSF1 and HSF3 cooperatively regulate the heat shock response in lizards. PLoS ONE 12:e0180776
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Tan JB, Macrae TH (2018) Stress tolerance in diapausing embryos of Artemia franciscana is dependent on heat shock factor 1 (Hsf1). PLoS ONE 13:e0200153
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Wan FH, Yang NW (2016) Invasion and management of agricultural alien insects in China. Annu Rev Entomol 61:77–98
Wang ZG, Guan W, Chen DH (2007) Preliminary report of the Liriomyza trifolii in Zhongshan area. Plant Quarantine 21:19–20
Wang HH, Reitz SR, Xiang JC, Smagghe G, Lei ZR (2014) Does Temperature-mediated reproductive success drive the direction of species displacement in two invasive species of leafminer fly? PLoS ONE 9:e98761
Wang HH, Rreitz S, Wang LX, Wang SY, Xue LI, 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. J Integr Agric 13:2196–2210
Wen JZ, Wang Y, Lei ZR (1996) New record of Liriomyza sativae Blanchard (Diptera: Agromyzidae) from China. Entomotaxonomia 18:311–312
Wen JZ, Lei ZR, Wang Y (1998) Survey of Liriomyza huidobrensis in Yunnan Province and Guizhou Province, China. Plant Prot 24:18–20
Wiederrecht G, Seto D, Parker CS (1988) Isolation of the gene encoding the S. cerevisiae heat shock transcription factor. Cell 6:841–853
Wu C (1995) Heat shock transcription factors: structure and regulation. Annu Rev Cell Dev Biol 1:441–469
Xiang JC, Lei ZR, Wang HH (2012) Interspecific competition among three invasive Liriomyza species. Acta Ecol Sin 32:1616–1622
Yan H, Zhang S, Li XY, Yuan FH, Qiu W, Chen YG, Weng SP, He JG, Chen YH (2014) Identification and functional characterization of heat shock transcription factor1 in Litopenaeus vannamei. Fish Shellfish Immun 37:184–192
Zhang XX, Qin J, Yuan JW, Lu MX, Du YZ (2019) Cloning of a new HSP70 gene from western flower thrips, Frankliniella occidentalis, and expression patterns during thermal stress. Peer J 7:e7687
Acknowledgements
This research was funded by the earmarked fund for Jiangsu Agricultural Industry Technology System (JATS [2020] 309), the Jiangsu Science & Technology Support Program (BE2014410), and the postgraduate Research & Practice Innovation Program of Jiangsu Province (KYCX18_2374).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Chang, YW., Wang, YC., Zhang, XX. et al. 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 (2021). https://doi.org/10.1007/s12192-021-01224-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12192-021-01224-2