Eur. J. Entomol. 121: 54-63, 2024 | DOI: 10.14411/eje.2024.008

Functional analysis of two SfHsp90 genes in response to high temperature and insecticide stress in Spodoptera frugiperda (Lepidoptera: Noctuidae)Original article

Hong-Yun RUAN ORCID...1, Lv ZHOU ORCID...1, Lei YANG ORCID...2, Jian-Yu MENG ORCID...3, Chang-Yu ZHANG ORCID...1,*
1 Guizhou Provincial Key Laboratory for Agricultural Pest Management of the Mountainous Region, Institute of Entomology, Guizhou University, Guiyang 550025, China; e-mails: 2398835118@qq.com (H.-Y. R.), 1269560136@qq.com (L.Z.), gzuzcy1121@126.com (C.-Y. Z)
2 China Tobacco Hunan Industrial Co., Ltd, Changsha, 410007, China; e-mail: 1092518523@qq.com (L.Y.)
3 Guizhou Tobacco Science Research Institute, Guiyang 550081, China; e-mail: mengjy0417@163.com (J.-Y. M.)

Spodoptera frugiperda, a worldwide pest, can feed on 353 crops species, including corn, rice, and sorghum. It is highly adaptable to various environments. Heat shock protein 90 kDa (Hsp90) plays a crucial role in the environmental adaptation of insects. To explore the role of SfHsp90 genes coding for Hsp90 proteins in the high temperature and insecticides stress resistance of Spodoptera frugiperda, we identified the complete complementary DNA sequences of two SfHsp90s. Both of them were expressed at different developmental stages and tissues in S. frugiperda. The expression levels of the SfHsp90s were significantly upregulated when exposed to durations of extreme temperature (45°C) and lethal concentrations of emamectin benzoate (LC10 and LC20). The viability of S. frugiperda under 45°C and emamectin benzoate stresses was examined. The mortality rate of S. frugiperda was significantly increased when subjected to 45°C and emamectin benzoate after knockdown of SfHsp90s by RNAi. These results suggest that SfHsp90s are essential for the resistance of S. frugiperda to high temperature and emamectin benzoate stresses.

Keywords: Crop pest, heat shock protein 90, knockdown, RNAi, emamectin benzoate, resistance

Received: November 27, 2023; Revised: January 23, 2024; Accepted: January 23, 2024; Published online: February 20, 2024  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
RUAN, H., ZHOU, L., YANG, L., MENG, J., & ZHANG, C. (2024). Functional analysis of two SfHsp90 genes in response to high temperature and insecticide stress in Spodoptera frugiperda (Lepidoptera: Noctuidae). EJE121, Article 54-63. https://doi.org/10.14411/eje.2024.008
Download citation

References

  1. Bauerfeind S.S. & Fischer K. 2014: Simulating climate change: temperature extremes but not means diminish performance in a widespread butterfly. - Popul. Ecol. 56: 239-250. Go to original source...
  2. 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. et al. 2002: Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. - Glob. Change Biol. 8: 1-16. Go to original source...
  3. Boaventura D., Martin M., Pozzebon A. Mota-Sanchez D. & Nauen R. 2020: Monitoring of target-site mutations conferring insecticide resistance in Spodoptera frugiperda. - Insects 11: 545, 15 pp. Go to original source...
  4. Brom K.R., Dolezych B., Tarnawska M., Brzozowska K. & Nakonieczny M. 2015: Expression of the Hsp40, Hsp70 and Hsp90 proteins in Colorado potato beetle (Leptinotarsa decemlineata Say) after the dimethoate treatment. - J. Entomol. Res. Soc. 17: 39-49.
  5. Carvalho R.A., Omoto C., Field L.M., Williamson M.S. & Bass C. 2013: Investigating the molecular mechanisms of organophosphate and pyrethroid resistance in the fall armyworm Spodoptera frugiperda. - PLoS ONE 8: e62268, 11 pp. Go to original source...
  6. Chen B. & Wagner A. 2012: Hsp90 is important for fecundity, longevity, and buffering of cryptic deleterious variation in wild fly populations. - BMC Evol. Biol. 12: 1-16. Go to original source...
  7. Chen B., Kayukawa T., Monteiro A. & Ishikawa Y. 2005: Theexpression of the HSP90 gene in response to winter and summer diapauses and thermal-stress in the onion maggot, Delia antiqua. - Insect Mol. Biol. 14: 697-702. Go to original source...
  8. Chen L.Z., Liang G.M., Zhang J., Wu K.M., Guo Y.Y. & Rector B.G. 2010: Proteomic analysis of novel Cry1Ac binding proteins in Helicoverpa armigera (Hübner). - Arch. Insect biochem. 73: 61-73. Go to original source...
  9. Chen X., Li Z.D., Dai Y.T., Jiang M.X. & Zhang C.X. 2020: Identification and characterization of three heat shock protein 90 (Hsp90) homologs in the brown planthopper. - Genes (Basel) 11: 1074, 15 pp. Go to original source...
  10. Cheng W.N., Li D., Wang Y., Liu Y. & Zhu-Salzman K. 2016: Cloning of heat shock protein genes (hsp70, hsp70 and hsp90) and their expression in response to larval diapause and thermal stress in the wheat blossom midge, Sitodiplosis mosellana. - J. Insect Physiol. 95: 66-77. Go to original source...
  11. Chown S.L. & Terblanche J.S. 2006: Physiological diversity in insects: ecological and evolutionary contexts. - Adv. Insect Physiol. 33: 50-152. Go to original source...
  12. Deutsch C.A., Tewksbury J.J., Huey R.B., Sheldon K.S., Ghalambor C.K., Haak D.C. & Martin P.R. 2008: Impacts of climate warming on terrestrial ectotherms across latitude. - Proc. Natl. Acad. Sci. USA 105: 6668-6672. Go to original source...
  13. Ding J.H., Zheng L.X., Chu J., Liang X.H., Wang J., Gao X.W., Wu F.A. & Sheng S. 2021: Characterization, and functional analysis of Hsp70 and Hsp90 gene families in Glyphodes pyloalis Walker (Lepidoptera: Pyralidae). - Front. Physiol. 12: 753914, 17 pp. Go to original source...
  14. Dumas P., Morin M.D., Boquel S., Moffat C.E. & Morin P.J. 2019: Expression status of heat shock proteins in response to cold, heat, or insecticide exposure in the Colorado potato beetle Leptinotarsa decemlineata. - Cell Stress Chaperon. 24: 539-547. Go to original source...
  15. Duncan R.F. 2005: Inhibition of Hsp90 function delays and impairs recovery from heat shock. - FEBS J. 272: 5244-5256. Go to original source...
  16. Farahani S., Bandani A.R., Alizadeh H., Goldansaz S.H. & Whyard S. 2020: Differential expression of heat shock proteins and antioxidant enzymes in response to temperature, starvation, and parasitism in the carob moth larvae, Ectomyelois ceratoniae (Lepidoptera: Pyralidae). - PLoS ONE 15: e0228104, 18 pp. Go to original source...
  17. Feder M.E. & Hofmann G.E. 1999: Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. - Annu. Rev. Physiol. 61: 243-282. Go to original source...
  18. Gao P., Jia X.F. & Wang H.P. 2016: Cloning and sequence analysis of Hsp90 and Hsp70 gene from Carposina sasakii Matsumura under heat stress. - J. Shenyang Agric. Univ. 47: 474-478.
  19. Guo X.J. & Feng J.N. 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. - J. Insect Sci. 18: 15, 10 pp. Go to original source...
  20. Gupta R.S. 1995: Phylogenetic analysis of the 90 kD heat shock family of protein sequences and an examination of the relationship among animals, plants, and fungi species. - Mol. Biol. Evol. 12: 1063-1073.
  21. Gutiérrez-Moreno R., Mota-Sanchez D., Blanco C.A., Whalon M.E., Terán-Santofimio H., Rodriguez-Maciel J.C. & DiFonzo C. 2019: Field-evolved resistance of the fall armyworm (Lepidoptera: Noctuidae) to synthetic insecticides in Puerto Rico and Mexico. - J. Econ. Entomol. 112: 792-802. Go to original source...
  22. Jiang J.J., Huang L.F., Li L.F., Chen H.S., Wang F.Y. & Yang L. 2019: Cloning and expression of the Bactrocera cucurbitae (Coquillett) heat shock protein 90 gene. - Chin. J. Appl. Entomol. 56: 444-453.
  23. Kampinga H.H., Hageman J., Vos M.J., Kubota H., Tanguay R.M., Bruford E.A., Cheetham M.E., Chen B. & Hightower L.E. 2009: Guidelines for the nomenclature of the human heat shock proteins. - Cell Stress Chaperon. 14: 105-111. Go to original source...
  24. King A.M. & MacRae T.H. 2015: Insect heat shock proteins during stress and diapause. - Annu. Rev. Entomol. 60: 59-75. Go to original source...
  25. Krishnamoorthy M., Jurat-Fuentes J.L., McNall R.J., Andacht T. & Adang M.J. 2007: Identification of novel Cry1Ac binding proteins in midgut membranes from Heliothis virescens using proteomic analyses. - Insect Biochem. Mol. Biol. 37: 189-201. Go to original source...
  26. Kumar S., Stecher G. & Tamura K. 2016: MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. - Mol. Biol. Evol. 33: 1870-1874. Go to original source...
  27. Li Y.T., Zhao Q., Fang B. & Chen M.H. 2017: Molecular cloning and expression analysis of the Hsp90 gene in the bird cherry-oat aphid, Rhopalosiphum padi. - J. Plant Prot. 44: 16-23.
  28. Lira E.C., Bolzan A., Nascimento A.R., Amaral F.S., Kanno R.H., Kaiser I.S. & Omoto C. 2020: Resistance of Spodoptera frugiperda (Lepidoptera: Noctuidae) to spinetoram: inheritance and cross-resistance to spinosad. - Pest Manag. Sci. 76: 2674-2680. Go to original source...
  29. Livak K.J. & Schmittgen T.D. 2011: Analysis of relative gene expression data using realtime quantitative PCR and the 2-ΔΔCt method. - Methods 25: 402-408. Go to original source...
  30. Mayer M.P. 2010: Gymnastics of molecular chaperones. - Mol. Cell 39: 321-331. Go to original source...
  31. Montezano D.G., Specht A., Sosa-Gómez D.R., Roque-Specht V.F., Sousa-Silva J.C., Paula-Moraes S.V., Peterson J.A. & Hunt T.E. 2018: Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the americas. - Afr. Entomol. 26: 286-300. Go to original source...
  32. Ohhara Y., Hoshino G., Imahori K., Matsuyuki T. & Yama­kawa-Kobayashi K. 2021: The nutrient-responsive molecular chaperone Hsp90 supports growth and development in Droso­phila. - Front. Physiol. 12: 690564, 12 pp. Go to original source...
  33. Pinto J.R.L., Torres A.F., Truzi C.C., Vieira N.F., Vacari A.M. & De Bortoli S.A. 2019: Artificial corn-based diet for rearing Spodoptera frugiperda (Lepidoptera: Noctuidae). - J. Insect Sci. 19: 2, 8 pp. Go to original source...
  34. Popović Ž.D., Subotić A., Nikolić T.V., Radojičić R., Blago­jević D.P., Grubor-Lajšić G. & Koštál V. 2015: Expression of stress-related genes in diapause of European corn borer (Ostrinia nubilalis Hbn.). - Comp. Biochem. Physiol. (B) 186: 1-7. Go to original source...
  35. Rinehart J.P., Li A., Yocum G.D., Robich R.M., Hayward S.A. & Denlinger D.L. 2007: Up-regulation of heat shock proteins is essential for cold survival during insect diapause. - Proc. Natl. Acad. Sci. USA 104: 11130-11137. Go to original source...
  36. 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. - Invert. Surviv. J. (Modena) 13: 350-354.
  37. Ruan H.Y., Meng J.Y., Yang C.L., Zhou L. & Zhang C.Y. 2022: Identification of six small heat shock protein genes in Ostrinia furnacalis (Lepidoptera: Pyralidae) and analysis of their expression patterns in response to environmental stressors. - J. Insect Sci. 22: 7, 13 pp. Go to original source...
  38. Rutherford S.L. & Lindquist S. 1998: Hsp90 as a capacitor for morphological evolution. - Nature 396: 336-342. Go to original source...
  39. Rutherford S., Knapp J.R. & Csermely P. 2007: Hsp90 and developmental networks. - Adv. Exp. Med. Biol. 594: 190-197. Go to original source...
  40. Shen J.R., Li M.F., Chen N.Z., Wang J.J. & Wan F.H. 2011: Cloning and analysis of the expression characteristics under heat stress of Hsp90 gene in the codling moth, Cydia pomonella (Lepidoptera: Tortricidae). - Acta Entomol. Sin. 54: 1236-1248.
  41. Shu Y., Du Y. & Wang J. 2011: Molecular characterization and expression patterns of Spodoptera litura heat shock protein 70/90, and their response to zinc stress. - Comp. Biochem. Physiol. (A) 158: 102-110. Go to original source...
  42. Sonoda S.J., 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. - Arch. Insect Biochem. Physiol. 62: 80-90. Go to original source...
  43. Su L., Meng J.Y., Zhu J.M. & Zhang C.Y. 2018: Cloning and expression of hsp90 gene from green peach aphid Myzus persicae under UV-B stress. - J. Plant Prot. 6: 1267-1273.
  44. 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 Chaperon. 19: 725-739. Go to original source...
  45. Tao Y.D., Liu Y., Wan X.S., Xu J., Fu D.Y. & Zhang J.Z. 2023: High and low temperatures differentially affect survival, reproduction, and gene transcription in male and female moths of Spodoptera frugiperda. - Insects 14: 958, 18 pp. Go to original source...
  46. Tian H., Yu S., Liu B., Yang J., Li X., Yue J. & Ran C. 2015: Molecular cloning of heat shock protein gene HSP90 and effects of abamectin and double-stranded RNA on its expression in Panonychus citri (Trombidiformes: Tetranychidae). - Fla Entomol. 98: 37-43. Go to original source...
  47. Todd E.L. & Poole R.W. 1980: Keys and illustrations for the armyworm moths of the noctuid genus Spodoptera Guenée from the western hemisphere. - Ann. Entomol. Soc. Am. 73: 722-738. Go to original source...
  48. 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). - J. Econ. Entomol. 108: 1313-1323. Go to original source...
  49. Tungjitwitayakul J., Tatun N., Vajarasathira B. & Sakurai S. 2016: Effects of Ultraviolet-C and microwave irradiation on the expression of heat shock protein genes in the maize weevil (Coleoptera: Curculionidae). - Eur. J. Entomol. 113: 135-142. Go to original source...
  50. Vatanparast M. & Park Y. 2022: Cold tolerance strategies of the fall armyworm, Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae). - Sci. Rep. 12: 4129, 16 pp. Go to original source...
  51. Wang H.H., Reitz S.R., Wang L.X., Wang S.Y., Li X. & 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. - J. Integr. Agr. 13: 2196-2210. Go to original source...
  52. Wei H.Y. & Du J.W. 2004: Sublethal effects of larval treatment with deltamethrin on moth sex pheromone communication system of the Asian corn borer, Ostrinia furnacalis. - Pestic. Biochem. Physiol. 80: 12-20. Go to original source...
  53. Wu Y.K., Zou C., Fu D.M., Zhang W.N. & Xiao H.J. 2018: Molecular characterization of three Hsp90 from Pieris and expression patterns in response to cold and thermal stress in summer and winter diapause of Pieris melete. - Insect Sci. 25: 273-283. Go to original source...
  54. Yang J., Nasir A.B. & Fan D. 2017: cDNA Cloning and induction of heat shock protein Hsp90 from Mythimna separata. - Chin. J. Biol. Contr. 33: 623-630.
  55. Zhai H.F., Jiang X.F. & Luo L.Z. 2010: Cloning and expression of Hsp90 cDNA in larvae of the beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae) under high temperature stress. - Acta Entomol. Sin. 53: 20-28.
  56. 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. - J. Insect Physiol. 56: 138-150. Go to original source...
  57. Zhang D.D. & Wu K.M. 2019: The bioassay of chinese domestic Bt-Cry1Ab and Bt-(Cry1Ab+Vip3Aa) maize against the fall armyworm, Spodoptera frugiperda. - Plant Prot. 45: 54-60.
  58. Zhang Q., Lu M.X. & Zhu S.D. 2014: Cloning, sequence analysis and expression profiling of heat shock protein 90 gene in the small brown plant hopper, Laodelphax striatellus (Hemiptera: Delphacidae). - Acta Entomol. Sin. 57: 777-786.

This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.