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Journal of Integrative Agriculture  2019, Vol. 18 Issue (1): 134-142    DOI: 10.1016/S2095-3119(18)61931-8
Special Issue: 害虫抗药性和毒理学合辑Pest Toxicology
Plant Protection Advanced Online Publication | Current Issue | Archive | Adv Search |
Effects of lead stress on Vg expression in the beet armyworm over five successive generations
SU Hong-hua, YANG Yong, QIAN Yuan-yuan, YE Zi-bo, CHEN Yu-qing, YANG Yi-zhong
School of Horticulture and Plant Protection, Yangzhou University, Yangzhou 225009, P.R.China
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Heavy metals have been found to be endocrine disruptors in invertebrates.  Lead is one of the most widespread elements of contamination, but there has been no research about the effects of lead stress on vitellogenin (Vg) gene expression in insects exposed to lead over multiple generations.  In this paper, the effects of different concentrations of lead (0, 0.3, 4.8 and 76.8 mg kg–1) on the expression of Vg in the beet armyworm over five successive generations were studied.  The results showed that lead stress had significant effects on Vg expression in a dose-dependent manner.  For females at the larval and adult stages, as lead concentration increased, Vg expression was significantly inhibited; for males at these two developmental stages, Vg expression was induced and increased as lead concentration increased.  In addition, with the increase over stressed generations, inhibited effects for females and induced effects for males at the larval and adult stages became increasingly more obvious.  However, at the pupal stage, Vg expression in the two genders was different from that at the larval and adult stages.  The results indicate that lead stress can upregulate Vg expression in males which should be a useful indicator for environmental risk assessment.
Keywords:  Spodoptera exigua        lead stress        vitellogenin        gene expression        females        males  
Received: 12 December 2017   Accepted:
Fund: This research was supported by the National Key Research and Development Program of China (2017YFD0201907), the National Science and Technology Major Project, China (2016ZX08012-004), and the Key Research and Development Project of Jiangsu Province, China (BE2017379-3).
Corresponding Authors:  Correspondence YANG Yi-zhong, E-mail:    
About author:  SU Hong-hua, Tel: +86-514-87979344, E-mail:;

Cite this article: 

SU Hong-hua, YANG Yong, QIAN Yuan-yuan, YE Zi-bo, CHEN Yu-qing, YANG Yi-zhong. 2019. Effects of lead stress on Vg expression in the beet armyworm over five successive generations. Journal of Integrative Agriculture, 18(1): 134-142.

Agnieszka J B, Ryszard L. 2008. Effects of nickel and temperature on the ground beetle Pterostichus oblongopunctatus (Coleoptera: Carabidae). Ecotoxicology, 17, 189–198.
Blariza M J, Leyria J, Canavoso L E, Soria N W, García B A. 2016. Dynamics of expression of two vitellogenin genes in the Chagas’ disease vector Triatoma infestans: Analysis throughout pre-vitellogenesis and vitellogenesis. Acta Tropica, 156, 100–107.
Bownes M. 1982. Hormonal and genetic regulation of vitellogenesis in Drosophila. The Quarterly Review of Biology, 57, 247–274.
Briers T, van Beek E, De Loof A. 1983. Ecdysteroid activity during metamorphosis and in male and female adults of four blowfly species. Comparative Biochemistry and Physiology (Part A: Physiology), 74, 521–524.
Buszczak M, Freeman M R, Carlson J R, Bender M, Cooley L, Segraves W A. 1999. Ecdysone response genes govern egg chamber development during mid-oogenesis in Drosophila. Development, 126, 4581–4589.
Cain D, Croteau M, Luomaz S. 2011. Bioaccumulation dynamics and exposure of Cd and Cu among species of aquatic mayflies. Environmental Toxicology and Chemistry, 30, 2532–2541.
Cervera A, Maymo A C, Mart?´nez-Pardo R, Garcera M D. 2005. Vitellogenesis inhibition in Oncopeltus fasciatus females (Heteroptera:Lygaeidae) exposed to cadmium. Journal of Insect Physiology, 51, 895–911.
Chen H, Teng Y, Lu S, Wang Y, Wang J. 2015. Contamination features and health risk of soil heavy metals in China. Science of the Total Environment, 512–513, 143–153.
Depledge M H, Billinghurst Z. 1999. Ecological significance of endocrine disruption in marine invertebrates. Marine Pollution Bulletin, 39, 32–38.
Donwheeler G, Engelmann F. 1997. The biosynthesis and processing of vitellogenin in the fat bodies of females and males of the cockroach Leucophaea maderae. Insect Biochemistry and Molecular Biology, 27, 901–918.
Engelmann F. 1979. Insect vitellogenin: Identification biosynthesis, and role in vitellogenesis. Advances in Insect Physiology, 14, 49–108.
Gao H, Zhao H, Du C, Deng M, Du E, Hu Z, Hu X. 2012. Life table evaluation of survival and reproduction of the aphid, Sitobion avenae, exposed to cadmium. Journal of Insect Science, 12, 44.
GB 2762-2005. 2005. National food safety standard, maximum levels of contaminants in foods. General Administration of Quality Supervision, Inspection and Qurantine of the China. (in Chinese)
Ge F. 2011. Challenges facing entomologists in a changing global climate. Chinese Journal of Applied Entomology, 48, 1117–1122. (in Chinese)
Hu M M, Cai W C, Su H H, Yang Y Z. 2014. Accumulation of lead in Spodoptera exigua (Hübner) and its impact on the population. Chinese Journal of Applied Ecology, 25, 1145–1150. (in Chinese)
Huang D, Kong J, Seng Y. 2012. Effects of the heavy metal Cu2+ on growth, development, and population dynamics of Spodoptera litura (Lepidoptera: Noctuidae). Journal of Economic Entomology, 105, 288–294.
Huybrechts R, De Loof A. 1977. Induction of vitellogenin synthesis in male Sarcophaga bullata by ecdysterone. Journal of Insect Physiology, 23, 1359–1362.
Jones R E. 1978. The vertebrate ovary. In: Comparative Biology and Evolution. Plenum Press, USA.
Kafel A, Rozp?dek K, Szulińska E, Zawisza-Raszka A, Migula P. 2014. The effects of cadmium or zinc multigenerational exposure on metal tolerance of Spodoptera exigua 
(Lepidoptera: Noctuidae). Environmental Science and Pollution Research International, 21, 4705–4715.
Kim K S, Funk D H, Buchwalter D B. 2012. Dietary (periphyton) and aqueous Zn bioaccumulation dynamics in the mayfly Centroptilum triangulifer. Ecotoxicology, 21, 2288–2296.
Lanot R, Thiebold J, Costet-Corio M F, Benveniste P, Hoffmann J A. 1988. Further experimental evidence for the involvement of ecdysone in the control of meiotic reinitiation in oocytes of Locusta migratoria (Insecta, Orthoptera). Development Biology, 126, 212–214.
Li J, Huang J, Cai W, Zhao Z, Peng W, Wu J. 2010. The vitellogenin of the bumblebee, Bombus hypocrita: studies on structural analysis of the cDNA and expression of the mRNA. Journal of Comparative Physiology (B: Biochemical, Systemic, and Environmental Physiology), 180, 161–170.
Li J L, Wu J, Cai W Z, Zhao Z W. 2009. The functions of vitellogenin in the honeybee. Chinese Bulletin of Entomology, 46, 802–806. (in Chinese)
Liang Q L, Yang H, Zhao L. 2013. The heavy metal contents in vegetables from Lishui City and the heath risk assessment. Northern Horticulture, 12, 21–24. (in Chinese)
Liu C Y. 2013. Function of vitellogenin gene in Chrysopa septempunctata. Ph D thesis, Chinese Academy of Agricultural Sciences, Beijing. (in Chinese)
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-??CT method. Methods, 25, 402–408.
Loeb M J, De Loof A, Gelman D B. 2001. Testis ecdysiotropin, an insect gonadotropin that induces synthesis of ecdysteroid. Archives of Insect Biochemistry and Physiology, 47, 181–188.
De Loof A. 2006. Ecdysteroids: The overlooked sex steroids of insects? Males: The black box. Insect Science, 13, 325–338.
Lu K, Chen X, Liu W T, Zhang X Y, Chen M X, Zhou Q. 2016. Nutritional signaling regulates vitellogenin synthesis and egg development through juvenile hormone in Nilaparvata lugens (Stål). International Journal of Molecular Sciences, 17, 269.
Martín-Díaz M L, Sales D, DelValls A. 2008. Toxicokinetic approach for the assessment of endocrine disruption effects of contaminated dredged material using female Carcinus maenas. Ecotoxicology, 17, 495–503.
Martín-Díaz M L, Villena-Lincoln A, Bamber S, Blasco J, DelValls T A. 2005. An integrated approach using bioaccumulation and biomarker measurements in female shorecrab, Carcinus maenas. Chemosphere, 58, 615–626.
Matozzo V, Gagné F, Marin M G, Ricciardi F, Blaise C. 2008. Vitellogenin as a biomarker of exposure to estrogenic compounds in aquatic invertebrates: A review. Environment International, 34, 531–545.
Piulachs M D, Guidugli K R, Barchuk A R, Cruz J, Simões Z L, Bellés X. 2003. The vitellogenin of the honey bee, Apis mellifera: Structural analysis of the cDNA and expression studies. Insect Biochemistry and Molecular Biology, 33, 459–465.
Salice C J, Miller T J, Roesijadi G. 2009. Demographic 
responses to multigeneration cadmium exposure in two strains of the freshwater gastropod, Biomphalaria glabrata. Archives of Environmental Contamination and Toxicology, 56, 785–795.
Shu Y H, Zhou J L, Tang W C, Lu K, Zhou Q, Zhang G R. 2009. Molecular characterization and expression pattern of Spodoptera litura (Lepidoptera: Noctuidae) vitellogenin, and its response to lead stress. Journal of Insect Physiology, 55, 608–616.
Su H H, Hu M M, Harvey-Samuel T, Yang Y Z. 2014. Accumulation and excretion of cadmium in three successive generations of Spodoptera exigua (Hübner) and impact on the population increase. Journal of Economic Entomology, 107, 223–229.
Tufail M, Le J M, Hatakeyama M, Oishi K, Takeda M. 2000. Cloning of vitellogenin cDNA of the American cockroach, Periplaneta americana (Dictyoptera), and its structural and expression analyses. Archives of Insect Biochemistry and Physiology, 45, 37–46.
Tufail M, Naeemullah M, Elmogy M, Sharma P N, Takeda M, Nakamura C. 2010. Molecular cloning, transcriptional regulation, and differential expression profiling of vitellogenin in two wing-morphs of the brown planthopper, Nilaparvata lugens Stål (Hemiptera: Delphacidae). Insect Molecular Biology, 19, 787–798.
Wan T L, Liu S, Tang Q Y, Cheng J A. 2014. Heavy metal bioaccumulation and mobility from rice plants to Nilaparvata lugens (Homoptera: Delphacidae) in China. Environmental Entomology, 43, 654–661.
Wang X H, Xu H F, Xu Y Y, Liu Y, Zhou Z. 2003. Reproductive system structure of Spodoptera exigua female, development classification and the application in forecasting. Acta Phytophylacica Sinica, 30, 261–266. (in Chinese)
Xie G, Zou J, Zhao L, Wu M, Wang S, Zhang F, Tang B. 2014. Inhibitional effects of metal Zn2+ on the reproduction of Aphis medicaginis and its predation by Harmonia axyridis. PLoS ONE, 9, e87639.
Xu B. 2012. Research on the morphological structure and development of Spodoptera litura prothoracic glands and gonads. MSc thesis, Zhongshan University, Guangzhou. (in Chinese)
Yan Y, Peng L, Wan F H. 2010. Pleiotrophic functions of insect Vitellogenin: With honeybee Apis mellifera as an example. Acta Entomologica Sinica, 53, 335–348. (in Chinese)
Zhang H H. 2015. Pollution effects of heavy metals in dry deposition on soil-vegetable system in suburban Shanghai. MSc thesis, East China Normal University, Shanghai. (in Chinese)
Zhang Y P, Sun G, Wang Y, Yang H M, Li L J, Ma E B, Guo Y P. 2011. Cadmium and chromium accumulation in the tissues of the Chinese rice grasshopper, Oxya chinensis. Journal of Agro-Environment Science, 30, 2440–2445. (in Chinese)
Zhang Z W, Lu X G, Wang Q C, Zheng D M. 2009. Mercury, cadmium and lead biogeochemistry in the soil-plant-insect system in Huludao City. Bulletin of Environmental Contamination and Toxicology, 83, 255–259.
Zhao J, Sun Y, Xiao L, Tan Y, Bai L. 2016. Molecular characterization and expression of vitellogenin gene from Spodoptera exigua exposed to cadmium stress. Gene, 593, 179–184.
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