Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-22T04:34:27.074Z Has data issue: false hasContentIssue false
  • English
  • Français

Characterization, expression profiling, and thermal tolerance analysis of heat shock protein 70 in pine sawyer beetle, Monochamus alternatus hope (Coleoptera: Cerambycidae)

Published online by Cambridge University Press:  16 September 2020

Hui Li ,
Heng Qiao ,
Yujie Liu ,
Shouyin Li ,
Jiajin Tan  and
Dejun Hao Open the ORCID record for Dejun Hao [Opens in a new window]
Hui Li
Affiliation:
Co-Innovation Center for the Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing, China College of Forestry, Nanjing Forestry University, Nanjing, China
Heng Qiao
Affiliation:
Co-Innovation Center for the Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing, China College of Forestry, Nanjing Forestry University, Nanjing, China
Yujie Liu
Affiliation:
Co-Innovation Center for the Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing, China College of Forestry, Nanjing Forestry University, Nanjing, China
Shouyin Li
Affiliation:
Co-Innovation Center for the Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing, China College of Forestry, Nanjing Forestry University, Nanjing, China
Jiajin Tan
Affiliation:
Co-Innovation Center for the Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing, China College of Forestry, Nanjing Forestry University, Nanjing, China
Dejun Hao*
Affiliation:
Co-Innovation Center for the Sustainable Forestry in Southern China, Nanjing Forestry University, Nanjing, China College of Forestry, Nanjing Forestry University, Nanjing, China
*
Author for correspondence: Dejun Hao, Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Monochamus alternatus Hope (Coleoptera: Cerambycidae) warrants attention as a dominant transmission vector of the pinewood nematode, and it exhibits tolerance to high temperature. Heat shock protein 70 (HSP70) family members, including inducible HSP70 and heat shock cognate protein 70 (HSC70), are major contributors to the molecular chaperone networks of insects under heat stress. In this regard, we specifically cloned and characterized three MaltHSP70s and three MaltHSC70s. Bioinformatics analysis on the deduced amino acid sequences showed these genes, having close genetic relationships with HSP70s of Coleopteran species, collectively shared conserved signature structures and ATPase domains. Subcellular localization prediction revealed the HSP70s of M. alternatus were located not only in the cytoplasm and endoplasmic reticulum but also in the nucleus and mitochondria. The transcript levels of MaltHSP70s and MaltHSC70s in each state were significantly upregulated by exposure to 35–50°C for early 3 h, while MaltHSP70s reached a peak after exposure to 45°C for 2–3 h in contrast to less-upregulated MaltHSC70s. In terms of MaltHSP70s, the expression threshold in females was lower than that in males. Also, both fat bodies and Malpighian tubules were the tissues most sensitive to heat stress in M. alternatus larvae. Lastly, the ATPase activity of recombinant MaltHSP70-2 in vitro remained stable at 25–40°C, and this recombinant availably enhanced the thermotolerance of Escherichia coli. Overall, our findings unraveled HSP70s might be the intrinsic mediators of the strong heat tolerance of M. alternatus due to their stabilized structure and bioactivity.

Keywords

ATPase activityexpression analysisheat shock protein 70Monochamus alternatusthermotolerance
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 2 , April 2021 , pp. 217 - 228
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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

Arrese, EL and Soulages, JL (2010) Insect fat body: energy, metabolism, and regulation. Annual Review of Entomology 55, 207–225.CrossRefGoogle ScholarPubMed
Cai, Z, Chen, J, Cheng, J and Lin, T (2017) Overexpression of three heat shock proteins protects Monochamus alternatus (Coleoptera: Cerambycidae) from thermal stress. Journal of Insect Science 17, 1–17.CrossRefGoogle Scholar
Chandrakanth, N, Ponnuvel, KM, Moorthy, SM, Sasibhushan, S and Sivaprasad, V (2015) Analysis of transcripts of heat shock protein genes in silkworm, Bombyx mori (Lepidoptera: Bombycidae). European Journal of Entomology 112, 676–687.CrossRefGoogle Scholar
Chang, YW, Zhang, XX, Chen, JY, Lu, MX, Gong, WR and Du, YZ (2018) Characterization of three heat shock protein 70 genes from Liriomyza trifolii and expression during thermal stress and insect development. Bulletin of Entomological Research 109, 1–10.Google ScholarPubMed
Chen, H, Xu, XL, Li, YP and Wu, JX (2014) Characterization of heat shock protein 90, 70 and their transcriptional expression patterns on high temperature in adult of Grapholita Molestar (Busck). Insect Science 21, 439–448.CrossRefGoogle Scholar
Chen, M, Zhang, N, Jiang, H, Meng, X, Qiang, K and Wang, J (2020) Transcriptional regulation of heat shock protein 70 genes by class i histone deacetylases in the red flour beetle, Tribolium castaneum. Insect Molecular Biology 29, 221–230.CrossRefGoogle ScholarPubMed
Cheng, WN, Li, D, Wang, Y, Liu, Y and Keyan, ZS (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.CrossRefGoogle ScholarPubMed
Chuvakova, LN, Sharko, FS, Nedoluzhko, AV, Polilov, AA, Prokhorchuk, EB, Skryabin, KG and Evgen'ev, MB (2017) Hsp70 genes of the Megaphragma Amalphitanum (Hymenoptera: trichogrammatidae) parasitic wasp. Molecular Biology 51, 615–621.CrossRefGoogle ScholarPubMed
Crack, JA, Mansour, M, Sun, Y and MacRae, TH (2002) Functional analysis of a small heat shock/alpha-crystallin protein from Artemia franciscana. European Journal of Biochemistry 269, 933–942.CrossRefGoogle ScholarPubMed
Daugaard, M, Rohde, M and Marja, J (2007) The heat shock protein 70 family: highly homologous proteins with overlapping and distinct functions. FEBS Letters 581, 3702–3710.CrossRefGoogle ScholarPubMed
Economou, K, Kotsiliti, E and Mintzas A, C (2017) Stage and cell-specific expression and intracellular localization of the small heat shock protein Hsp27 during oogenesis and spermatogenesis in the Mediterranean fruit fly, Ceratitis capitata. Journal of Insect Physiology 96, 64–72.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
Flaherty, KM, DeLuca-Flaherty, C and McKay, D (1990) Three-dimensional structure of the ATPase fragment of a 70K heat-shock cognate protein. Nature 346, 623–628.CrossRefGoogle ScholarPubMed
Garrad, R, Booth, DT and Furlong, MJ (2016) The effect of rearing temperature on development, body size, energetics and fecundity of the diamondback moth. Bulletin of Entomological Research 1, 1–7.Google Scholar
Giannetto, A, Oliva, S, Mazza, L, Mondelo, G, Savastano, D, Mauceri, A and Fasulo, S (2017) Molecular characterization and expression analysis of, heat shock protein 70, and, 90, from, Hermetia Illucens, reared in a food waste bioconversion pilot plant. Gene 627, 15–25.CrossRefGoogle Scholar
González-Tokman, D, Córdoba-Aguilar, A, Dáttilo, W, Lira-Noriega, A, Sánchez-Guillén, RA and Villalobos, F (2020) Insect responses to heat: physiological mechanisms, evolution and ecological implications in a warming world. Biological Reviews 95, 802–821.CrossRefGoogle Scholar
Guo, XJ and Nian, FJ (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, 1–10.CrossRefGoogle ScholarPubMed
Hartl, FU and Hayer-Hartl, M (2002) Protein folding molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295, 1852–1858.CrossRefGoogle ScholarPubMed
Hu, LJ and Wu, XQ (2018) Research progress on the mechanism of pine response to the infection of Bursaphelenchus xylophilus. Chinese Bulletin of Life Science 30, 559–666.Google Scholar
Huang, LH, Wang, HS and Kang, L (2008) Different evolutionary lineages of large and small heat shock proteins in eukaryotes. Cell Research 18, 1074–1076.CrossRefGoogle ScholarPubMed
Huang, LH, Wang, CZ and 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.CrossRefGoogle ScholarPubMed
Jinwal, UK, Miyata, Y, Koren, J, Jones, JR, Trotter, JH, Chang, L, O,Leary, J, Morgan, D, Lee, DC, Shults, CL, Rousaki, A, Weeber, EJ, Zuiderweg, ERP, Gestwicki, JE and Dickey, CA (2009) Chemical manipulation of hsp70 ATPase activity regulates tau stability. Journal of Neuroscience 29, 12079–12088.CrossRefGoogle ScholarPubMed
Kim, YE, Hipp, MS, Bracher, A, Hayer-Hartl, M and Hartl, FU (2013) Molecular chaperone functions in protein folding and proteostasis. Annual Review of Biochemistry 82, 323–355.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, M, Lu, WC, Feng, HZ and He, L (2009) Molecular characterization and expression of three heat shock protein70 genes from the carmine spider mite, Tetranychus cinnabarinus (boisduval). Insect Molecular Biology 18, 183–194.CrossRefGoogle Scholar
Li, H, He, XY, Tao, R, Gong, XY, Chen, HJ and Hao, DJ (2018) cDNA cloning and expression profiling of small heat shock protein genes and their response to temperature stress in Monochamus alternatus (Coleoptera: Cerambycidae). Acta Entomologica Sinica 61, 749–760.Google Scholar
Li, H, Zhao, XY, Qiao, H, He, XY, Tan, JX and Hao, DJ (2020) Comparative transcriptome analysis of the heat stress response in Monochamus alternatus hope (Coleoptera: Cerambycidae). Frontiers in Fhysiology 10, 1568.CrossRefGoogle Scholar
Lin, BL, Wang, JS, Liu, HC, Chen, RW, Meyer, Y, Barakat, A and Delseny, M (2001) Genomic analysis of the Hsp70 superfamily in Arabidopsis thaliana. Cell Stress & Chaperones 6, 201–208.2.0.CO;2>CrossRefGoogle ScholarPubMed
Linit, MJ (1988) Nemtaode-vector relationships in the pine wilt disease system. Journal of Nematology 20, 227–235.Google ScholarPubMed
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-△△CT method. Methods 25, 402–408.CrossRefGoogle Scholar
Luo, S, Ahola, V, Shu, C, Xu, C and Wang, R (2015) Heat shock protein 70 gene family in the Glanville Fritillary butterfly and their response to thermal stress. Gene 556, 132–141.CrossRefGoogle ScholarPubMed
Mamiya, Y and Enda, N (1979) Bursaphelenchus mucronatus n.sp. (Nematoda: Aphelenchoididae) from pine wood and its biology and pathogenicity to pine trees. Nematologica 25, 353–361.CrossRefGoogle Scholar
Mashaghi, A, Bezrukavnikov, S, Minde, DP, Wentink, AS, Kityk, R, Zachmann-Brand, B, Mayer, MP, Kramer, G, Bukau, B and Tans, SJ (2016) Alternative modes of client binding enable functional plasticity of Hsp70. Nature 539, 448–451.CrossRefGoogle ScholarPubMed
Matthias, PM and Gierasch, GM (2019) Recent advances in the structural and mechanistic aspects of Hsp70 molecular chaperones. Journal of Biological Chemistry 294, 2085–2097.Google Scholar
Paine, PL, Moore, LC and Horowitz, SB (1975) Nuclear envelope permeability. Nature 254, 109–114.CrossRefGoogle ScholarPubMed
Pockley, AG (2003) Heat shock proteins as regulators of the immune response. Lancet 362, 469–476.CrossRefGoogle ScholarPubMed
Prentice, HM, Milton, SL, Scheurle, D and Lutz, PL (2004) The upregulation of cognate and inducible heat shock proteins in the anoxic turtle brain. Journal of Cerebral Blood Flow and Metabolism 24, 826e828.CrossRefGoogle ScholarPubMed
Qin, WS, Tyshenko, MJ, Wu, BS, Walker, VK and Robertson, RM (2003) Cloning and characterization of a member of the hsp70 gene family from Locusta Migratoria, a highly thermotolerant insect. Cell Stress & Chaperones 8, 144–152.2.0.CO;2>CrossRefGoogle ScholarPubMed
Quan, GX, Duan, J, Ladd, T and Krell, PJ (2018) Identification and expression analysis of multiple small heat shock protein genes in spruce budworm, Choristoneura Fumiferana (L.). Cell Stress & Chaperones 23, 141–154.CrossRefGoogle Scholar
Ritossa, FM (1962) A new puffing pattern induced by temperature shock and dnp in drosophila. Experientia 18, 571–573.CrossRefGoogle Scholar
Rizana, M, Yan, ZK and Bhadriraju, S (2005) Changes in expression of heat shock proteins in Tribolium castaneum (Coleoptera: Tenebrionidae) in relation to developmental stage, exposure time, and temperature. Annals of the Entomological Society of America 98, 100–107.Google Scholar
Sakano, D, Li, B, Xia, Q, Yamamoto, K, Banno, Y, Fujii, H and Aso, Y (2006) Genes encoding small heat shock proteins of the silkworm, Bombyx mori. Bioscience Biotechnology and Biochemistry 70, 2443–2450.CrossRefGoogle ScholarPubMed
Shen, Y, Gu, J, Huang, LH, Zheng, SC, Liu, L, Xu, WH, Feng, QL and Kang, L (2011) Cloning and expression analysis of six small heat shock protein genes in the common cutworm, Spodoptera litura. Journal of Insect Physiology 57, 908–914.CrossRefGoogle ScholarPubMed
Sonoda, S, Fukumoto, K, Izumi, Y, Yoshida, H and Tsumuki, H (2006) Cloning of heat shock protein genes (hsp90 and hsc70) and their expression during larval diapause and cold tolerance acquisition in the rice stemborer, Chilo Suppressalis Walker. Archives of Insect Biochemistry and Physiology 63, 36–47.CrossRefGoogle Scholar
Sørensen, JG, Michalak, P, Justesen, J and Loeschcke, V (1999) Expression of the heat-shock protein HSP70 in Drosophila Buzzatii lines selected for thermal resistance. Hereditas 131, 155–164.CrossRefGoogle ScholarPubMed
Sorensen, JG, Kristensen, TN, Kristensen, KV and Loeschcke, V (2007) Sex specific effects of heat induced hormesis in HSF-deficient Drosophila melanogaster. Experimental Gerontology 42, 1123–1129.CrossRefGoogle ScholarPubMed
Stetler, RA, Gan, Y, Zhang, W, Liou, AK, Gao, Y, Cao, G and Chen, J (2010) Heat shock proteins: cellular and molecular mechanisms in the central nervous system. Progress in Neurobiology 92, 184–211.CrossRefGoogle ScholarPubMed
Sun, Y, Zhao, J, Sheng, Y, Xiao, YF, Zhang, YJ, Bai, LX, Tan, Y, Xiao, BL and Xu, GC (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.CrossRefGoogle ScholarPubMed
Tachibana, SI, Numata, H and Goto, SG (2005) Gene expression of heat-shock protein-s (hsp23, hsp70 and hsp90) during and after larval diapause in the blow fly Lucilia sericata. Journal of Insect Physiology 51, 641–647.CrossRefGoogle Scholar
Tamura, K, Peterson, D, Peterson, N, Stecher, G, Nei, G and Kumar, S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology & Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Udaka, H, Ueda, C and Goto, SG (2010) Survival rate and expression of Heat-shock protein 70 and Frost genes after temperature stress in Drosophila Melanogaster lines that are selected for recovery time from temperature come. Journal of Insect Physiology 56, 1889–1894.CrossRefGoogle Scholar
Vladimír, K, Michaela, TB and Marcelo, HL (2009) The 70 kda heat shock protein assists during the repair of chilling injury in the Pyrrhocoris apterus. Plos One 4, 45–46.Google Scholar
Wang, H, Dong, SZ, Li, K, Hu, C and Ye, GY (2008) A heat shock cognate 70 gene in the endoparasitoid, Pteromalus Puparum, and its expression in relation to thermal stress. Biochemistry and Molecular Biology Reports 41, 388–393.Google ScholarPubMed
Wang, H, Li, K, Zhu, JY, Fang, Q and Ye, GY (2012) Clonging and expression pattern of heat shock protein genes from the endoparasitoid wasp, Pteromalus Puparum inresponse to environmental stresses. Archives of Insect Biochemistry and Physiology 79, 247–263.CrossRefGoogle Scholar
Wang, H, Fang, Y, Bao, Z, Jin, X, Zhu, W, Wang, L, Liu, T, Ji, H, Wang, H, Xu, S and Sima, Y (2014) Identification of a Bombyx mori gene encoding small heat shock protein BmHsp27.4 expressed in response to high-temperature stress. Gene 538, 56–62.CrossRefGoogle ScholarPubMed
Wang, L, Yang, S, Zhao, K and Han, LL (2015) Expression profiles of the heat shock protein 70 gene in response to heat stress in Agrotis cnigrum (Lepidoptera: Noctuidae). Journal of Insect Science 15, 1–6.CrossRefGoogle Scholar
Wang, LH, Zhang, YL, Pan, L, Wang, Q, Han, YC, Niu, HT, Shan, D, Hoffmann, A and Fang, J (2019 a) Induced expression of small heat shock proteins is associated with thermotolerance in female Laodelphax striatellus planthoppers. Cell Stress & Chaperones 24, 115–123.CrossRefGoogle ScholarPubMed
Wang, XR, Wang, C, Ban, FX, Zhu, DT, Liu, SS and Wang, XW (2019 b) Genome-wide identification and characterization of HSP gene superfamily in whitefly (Bemisia tabaci) and expression profiling analysis under temperature stress. Insect Science 26, 44–57.CrossRefGoogle ScholarPubMed
Xin, TR, Lian, T, Li, XY, Li, L, Shen, QQ, Liu, XY and Xia, B (2018) Gene cloning and expression of heat shock protein gene from Aleuroglyphus ovatus and its response to temperature stress. International Journal of Acarology 44, 1–9.CrossRefGoogle Scholar
Xiong, Y, Liu, XQ, Xiao, PA, Tang, GH, Liu, SH, Lou, BH, Wang, JJ and Jiang, HB (2019) Comparative transcriptome analysis reveals differentially expressed genes in the Asian citrus psyllid (Diaphorina citri) upon heat shock. Comparative Biochemistry and Physiology - Part D 30, 256–261.Google ScholarPubMed
Yin, X, Wang, S, Tang, J, Hansen, JD and Lurie, S (2006) Thermal affects HSP70 ac-cumulation and insect mortality. Physiological Entomology 31, 241–247.CrossRefGoogle Scholar
Yu, CS, Lin, CJ and Hwang, JK (2004) Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions. Protein Science 13, 1402–1406.CrossRefGoogle ScholarPubMed
Zhang, Y, Liu, Y, Guo, X, Li, Y, Gao, H, Guo, X and Xu, B (2014) Shsp226, 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, YD, Zhou, Z, Wang, LG and Lin, G (2018) Transcriptome, expression, and activity analyses reveal a vital heat shock protein 70 in the stress response of stony coral Pocillopora damicornis. Cell Stress & Chaperones 23, 711–721.CrossRefGoogle ScholarPubMed
Zwirowski, S, Klosowska, A, Obuchowski, L, Nillegoda, N, Piróg, A, Ziętkiewicz, S, Bukau, B, Mogk, A and Liberek, K (2017) Hsp70 displaces small heat shock proteins from aggregates to initiate protein refolding. The EMBO Journal 36, 783–796.CrossRefGoogle ScholarPubMed
Supplementary material: File

Li et al. supplementary material

Li et al. supplementary material 1

Download Li et al. supplementary material(File)
File 46.6 KB
Supplementary material: File

Li et al. supplementary material

Li et al. supplementary material 2

Download Li et al. supplementary material(File)
File 3 MB
Supplementary material: File

Li et al. supplementary material

Li et al. supplementary material 3

Download Li et al. supplementary material(File)
File 49.7 KB
Supplementary material: File

Li et al. supplementary material

Li et al. supplementary material 4

Download Li et al. supplementary material(File)
File 32.3 KB