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| Susceptibility and tissue specificity of Spodoptera frugiperda to Junonia coenia densovirus |
CHEN Zu-wen1*, YANG Yan-chao1*, ZHANG Jian-feng1, JIN Ming-hui2, XIAO Yu-tao2, XIA Zhi-chao1, LIU Yuan-yuan1, YU Sai-zhen1, YANG Yong-bo1, WANG Yuan3, LI Yi4, LIU Kai-yu1 |
1 School of Life Sciences, Central China Normal University, Wuhan 430079, P.R.China
2 Agricultural Genomics Institute, Chinese Academy of Agricultural Sciences, Shenzhen 518120, P.R.China
3 Medical College, Hubei University of Arts and Science, Xiangyang 441053, P.R.China
4 Hubei Engineering Research Center of Viral Vector, Wuhan University of Bioengineering, Wuhan 430415, P.R.China |
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摘要
草地贪夜蛾又名秋行军虫，严重危害玉米和水稻等农作物，目前已经入侵我国。昆虫病毒作为生物农药，在控制害虫过程中具有重要的作用。昆虫浓核病毒具有环境友好和高效杀虫等优点，是一种潜在的生物杀虫剂。我们采用多种昆虫细胞系和鳞翅目昆虫幼虫从鹿眼蛱蝶浓核病毒全基因组感染性克隆成功拯救了病毒粒子。采用感染性克隆质粒转染的昆虫细胞系的匀浆物饲喂二龄草地贪夜蛾幼虫，具有致死效应。该浓核病毒感染致死的斜纹夜蛾的匀浆物对二龄草地贪夜蛾的半致死剂量是1.76×108 病毒基因组拷贝， 高于斜纹夜蛾（7.39×107 病毒基因组拷贝）和棉铃虫（9.71×107 病毒基因组拷贝）。这种匀浆物对草地贪夜蛾的半致死时间是6.96 d， 高于斜纹夜蛾（6.18）和棉铃虫（5.94 d）。该病毒能够感染棉铃虫的脂肪体，但是不能感染草地贪夜蛾和斜纹夜蛾的脂肪体。虽然这三种昆虫都对该病毒敏感，但是毒力大小具有差异。鹿眼蛱蝶浓核病毒可以作为控制草地贪夜蛾的潜在的生物杀虫剂。
Abstract The fall armyworm, Spodoptera frugiperda, which destroys many economic crops such as rice and maize, has recently invaded China. Insect viruses as biological control agents play important roles in killing pests. One potential viral insecticide is the environmentally highly infective and virulent densovirus. We successfully rescued Junonia coenia densovirus (JcDV) using its infectious clone in different insect cell lines and larvae of three insect species. Results showed that the lysate of cultured insect cells transfected by the JcDV infectious clone killed the 2nd instar S. frugiperda. The LD50 of homogenate from JcDV-infected Spodoptera litura to the 2nd instar S. frugiperda (1.76×108 viral genome copies per larva during 10 d post infection) was higher than that of the 2nd instar S. litura (7.39×107 JcDV genome copies) or Helicoverpa armigera larvae (9.71×107 JcDV genome copies). The LT50 of the S. litura homogenate (2.60×109 viral genome copies each larva) to the 2nd instar S. frugiperda was 6.96 d, longer than that of the S. litura (6.18 d) or the 2nd instar H. armigera (5.94 d). JcDV could infect the fat body of H. armigera, but not S. frugiperda or S. litura. Although JcDV can infect all three lepidopteran species, their susceptibility to the virus differs. JcDV has great potential as a biological control agent against pests such as S. frugiperda.
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Received: 30 August 2019
Accepted:
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| Fund: This work was supported by the National Key R&D Program of China (2017YFD0200400) and the Natural Science Foundation of Hubei Province, China (2017CFB241). |
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Corresponding Authors:
Correspondence LIU Kai-yu, E-mail: liukaiyu@mail.ccnu.edu.cn; LI Yi, E-mail: liyi@whsw.edu.cn
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| About author: * These authors contributed equally to this study. |
Cite this article:
CHEN Zu-wen, YANG Yan-chao, ZHANG Jian-feng, JIN Ming-hui, XIAO Yu-tao, XIA Zhi-chao, LIU Yuan-yuan, YU Sai-zhen, YANG Yong-bo, WANG Yuan, LI Yi, LIU Kai-yu.
2021.
Susceptibility and tissue specificity of Spodoptera frugiperda to Junonia coenia densovirus. Journal of Integrative Agriculture, 20(3): 840-849.
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Abd-Alla A, Jousset F X, Li Y, Fédière G, Cousserans F, Bergoin M. 2004. NS-3 protein of the Junonia coenia densovirus is essential for viral DNA replication in an Ld 652 cell line and Spodoptera littoralis larvae. Journal of Virology, 78, 790–797.
Barreau C, Jousset F X, Bergoin M. 1996. Pathogenicity of the Aedes albopictus parvovirus (AaPV), a denso-like virus, for Aedes aegypti mosquitoes. Journal of Invertebrate Pathology, 68, 299–309.
Belloncik S. 1990. Potential use of densonucleosis viruses as biological control agents of insect pests. In: Tijssen P, ed., Handbook of Parvoviruses. Vol. II. CRC Press, Boca Raton, Florida. pp. 285–289.
Bergoin M, Tijssen P. 2000. Molecular biology of densovirinae. Contributions to Microbiology, 4, 12–32.
Bruemmer A, Scholari F, Lopez-Ferber M, Conway J F, Hewat E A. 2005. Structure of an insect parvovirus (Junonia coenia densovirus) determined by cryo-electron microscopy. Journal of Molecular Biology, 347, 791–801.
Cotmore S F, Agbandje-McKenna M, Chiorini J A, Mukha D V, Pintel D J, Qiu J, Soderlund-Venermo M, Tattersall P, Tijssen P, Gatherer D, Davison A J. 2014. The family Parvoviridae. Archives of Virology, 159, 1239–1247.
Croizier L, Jousset F X, Veyrunes J C, López-Ferber M, Bergoin M, Croizier G. 2000. Protein requirements for assembly of virus-like particles of Junonia coenia densovirus in insect cells. Journal of General Virology, 81, 1605–1613.
Cuartas P E, Barrera G P, Belaich M N, Barreto E, Ghiringhelli P D, Villamizar L F. 2015. The complete sequence of the first Spodoptera frugiperda Betabaculovirus genome: A natural multiple recombinant virus. Viruses, 7, 394–421.
Davis T R, Wickham T J, McKenna K A, Granados R R, Shuler M L, Wood H A. 1993. Comparative recombinant production of eight insect lines. In Vitro Cellular & Developmental Biology, 29A, 388–390.
Ding C, Urabe M, Bergoin M, Kotin R M. 2002. Biochemical characterization of Junonia coenia densovirus nonstructural protein NS-1. Journal of Virology, 76, 338–345.
Dumas B, Jourdan M, Pascaud A M, Bergoin M. 1992. Complete nucleotide sequence of the cloned infectious genome of Junonia coenia densovirus reveals an organization unique among parvoviruses. Virology, 191, 202–222.
El-Mergawy R, Li Y, El-Sheikh M, El-Sayed M, Abol-Ela S, Bergoin M, Tjissen P, Fédière G. 2003. Epidemiology and biodiversity of the densovirus MlDV in the field populations of Spodoptera littoralis and other noctuid pests. Bulletin of Faculty of Agriculture (University of Cairo), 54, 269–282.
Escribano A, Williams T, Goulson D, Cave R D, Chapman J W, Caballero P. 1999. Selection of nucleopolyhedrovirus for control of Spodoptera frugiperda (Lepidoptera: Noctuidae): structural, genetic, and biological comparison of four isolates from the Americas. Journal of Economical Entomology, 92, 1079–1085.
Fédière G, El-Far M, Li Y, Bergoin M, Tijssen P. 2004. Expression strategy of densonucleosis virus from Mythimna loreyi. Virology, 320, 181–189.
Fédière G, Montsarrat P, Mariau D, Bergoin M. 1986. A densovirus of Casphalia extranea (Lepidoptera, Limacodidae): Characterization and use for biological control. In: Samson R A, Vlak J M, Peters D, eds., Fundamental and Applied Aspects of Invertebrate Pathology. The Foundation of the Fourth International Colloquium of Invertebrate Pathology, Wageningen. p. 705.
Ferrelli M L, Pidre M L, Ghiringhelli P D, Torres S, Fabre M L, Masson T, Cédola M T, Sciocco-Cap A, Romanowski V. 2018. Genomic analysis of an Argentinean isolate of Spodoptera frugiperda granulovirus reveals that various baculoviruses code for Lef-7 proteins with three F-box domains. PLoS ONE, 13, e0202598.
Gai Z, Zhang X, Islam M, Wang X, Li A, Yang Y, Li Y, Peng J, Hong H, Liu K. 2013. Characterization of Atg8 in lepidopteran insect cells. Archieves of Insect Biochemistry and Physiology, 84, 57–77.
Gasmi L, Frattini A, Ogliastro M, Herrero S. 2019. Outcome of mixed DNA virus infections on Spodoptera exigua susceptibility to SeMNPV. Journal of Pest Science, 92, 885–893.
Gasmi L, Jakubowska A K, Ferré J, Ogliastro M, Herrero S. 2018. Characterization of two groups of Spodoptera exigua Hübner (Lepidoptera: Noctuidae) C-type lectins and insights into their role in defense against the densovirus JcDV. Archives of Insect Biochemistry and Physiology, 97, e21432.
Jiang H, Zhang J M, Wang J P, Yang B, Liu C F, Lu J, Hu Y Y. 2007. Genetic engineering of Periplaneta fuliginosa densovirus as an improved biopesticide. Archieves of Virology, 152, 383–394.
Jiang H, Zhou L, Zhang J M, Dong H F, Hu Y Y, Jiang M S. 2008. Potential of Periplaneta fuliginosa densovirus as a biocontrol agent for smoky-brown cockroach, P. fuliginosa. Biological Control, 46, 94–100.
Jin M H, Tao J H, Li Q, Cheng Y, Sun X X, Wu K M, Xiao Y T. 2021. Genome editing of the SfABCC2 gene confers resistance to Cry1F toxin from Bacillus thuringiensis in Spodoptera frugiperda. Journal of Integrative Agriculture, 20, 815–820.
Jourdan M, Jousset F X, Gervais M, Skory S, Bergoin M, Dumas B. 1990. Cloning of the genome of a densovirus and rescue of infectious virions from recombinant plasmid in the insect host Spodoptera littoralis. Virology, 179, 403–409.
Kemmerer M, Bonning B C. 2020. Transcytosis of Junonia coenia densovirus VP4 across the gut epithelium of Spodoptera frugiperda (Lepidoptera: Noctuidae). Insect Science, 27, 22–32.
Kumar K K, Sridhar J, Murali-Baskaran R K, Senthil-Nathan S, Kaushal P, Dara S K, Arthurs S. 2019. Microbial biopesticides for insect pest management in India: Current status and futureprospects. Journal of Invertebrate Pathology, 165, 74–81.
Li Y, Jousset F X, Giraud C, Rolling F, Quiot J M, Bergoin M. 1996. A titration procedure of the Junonia coenia densovirus and quantitation of transfection by its cloned genomic DNA in four lepidopteran cell lines. Journal of Virology Methods, 57, 47–60.
Liu K, Li Y, Jousset F X, Zadori Z, Szelei J, Yu Q, Pham H T, Lépine F, Bergoin M, Tijssen P. 2011. The Acheta domesticus densovirus, isolated from the European house cricket, has evolved an expression strategy unique among parvoviruses. Journal of Virology, 85, 10069–10078.
Mutuel D, Ravallec M, Chabi B, Multeau C, Salmon J M, Fournier P, Ogliastro M. 2010. Pathogenesis of Junonia coenia densovirus in Spodoptera frugiperda: A route of infection that leads to hypoxia. Virology, 403, 137–144.
Nagoshi R N, Fleischer S, Meagher R L, Hay-Roe M, Khan A, Murua M G, Silvie P, Vergara C, Westbrook J. 2017. Fall armyworm migration across the Lesser Antilles and the potential for genetic exchanges between North and South American populations. PLoS ONE, 12, e0171743.
Okumura T, Matsumoto A, Tanimura T, Murakami R. 2005. An endoderm-specific GATA factor gene, dGATAe, is required for the terminal differentiation of the Drosophila endoderm. Developmental Biology, 278, 576–586.
Okumura T, Takeda K, Kuchiki M, Akaishi M, Taniguchi K, Adachi-Yamada T. 2016. GATAe regulates intestinal stem cell maintenance and differentiation in Drosophila adult midgut. Developmental Biology, 410, 24–35.
Pham H T, Huynh O T, Jousset F X, Bergoin M, Tijssen P. 2013. Junonia coenia densovirus (JcDNV) genome structure. Genome Announcement, 1, e00591–e00604.
Rivrse C F, Longwort J F. 1972. Nonoccluded virus of Junonia coenia (Nymphalidae: Lepidoptera). Journal of Invertebrate Pathology, 20, 369–370.
Salasc F, Mutuel D, Debaisieux S, Perrin A, Dupressoir T, Grenet A S, Ogliastro M. 2016. Role of the phosphatidylinositol-3-kinase/Akt/target of rapamycin pathway during ambidensovirus infection of insect cells. Journal of General Virology, 97, 233–245.
Schmittgen T D, Livak K J. 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3, 1101–1108.
Sharanabasappa K S, Asokan C M, Swamy R, Maruthi M S, Pavithra H B, Hegde K, Navi S, Prabhu S T, Goergen G. 2018. Fist report of the fall armyworm, Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), an alien invasive pest on maize in India. Pest Management in Horticultural Ecosystems, 24, 23–29.
Shapiro D I, Fuxa J R, Braymer H D, Pashley D P. 1991. DNA restriction polymorphism in wild isolates of Spodoptera frugiperda nuclear polyhedrosis virus. Journal of Invertebrate Pathology, 58, 96–105.
Smilanich A M, Langus T C, Doan L, Dyer L A, Harrison J G, Hsueh J, Teglas M B. 2018. Host plant associated enhancement of immunity and survival in virus infected caterpillars. Journal of Invertebrate Pathology, 151, 102–112.
Sun X L. 2015. History and current status of development and use of viral insecticides in China. Virus, 7, 306–319.
Sun X X, Zhao S Y, Jin M H, Zhao H Y, Li G P, Zhang H W, Jiang Y Y, Yang X M, Wu K M. 2019. Larval spatial distribution pattern and sampling technique of the fall armyworm Spodoptera frugiperda in maize fields. Plant Protection, 45, 13–18. (in Chinese)
Tijssen P, Li Y, El-Far M, Szelei J, Letarte M, Zádori Z. 2003. Organization and expression strategy of the ambisense genome of densonucleosis virus of Galleria mellonella. Journal of Virology, 77, 10357–10365.
Vendeville A, Ravallec M, Jousset F X, Devise M, Mutuel D, López-Ferber M, Fournier P, Dupressoir T, Ogliastro M. 2009. Densovirus infectious pathway requires clathrin-mediated endocytosis followed by trafficking to the nucleus. Journal of Virology, 83, 4678–4689.
Villamizar L, Barrera G, Cotes A M, Martínez F. 2010. Eudragit S100 microparticles containing Spodoptera frugiperda nucleopolyehedrovirus: Physicochemical characterization, photostability and in vitro virus release. Journal of Microencapsulation, 27, 314–324.
Wang L, Ma Y, Guo X, Wan P, Liu K, Cong S, Wang J, Xu D, Xiao Y, Li X, Tabashnik B E, Wu K. 2019. Pink bollworm resistance to Bt toxin Cry1Ac associated with an insertion in cadherin exon 20. Toxins, 11, 186.
Wang Y, Gosselin Grenet A S, Castelli I, Cermenati G, Ravallec M, Fiandra L, Debaisieux S, Multeau C, Lautredou N, Dupressoir T, Li Y, Casartelli M, Ogliastro M. 2013. Densovirus crosses the insect midgut by transcytosis and disturbs the epithelial barrier function. Journal of Virology, 87, 12380–12391.
Wei W, Pan S, Ma Y, Xiao Y, Yang Y, He S, Bravo A, Soberón M, Liu K. 2019. GATAe transcription factor is involved in Bacillus thuringiensis Cry1Ac toxin receptor gene expression inducing toxin susceptibility. Insect Biochemistry and Molecular Biology, 118, 103306.
Zhang L, Liu B, Jiang Y, Liu J, Wu K, Xiao Y. 2020. Molecular characterization analysis of fall armyworm populations in China. Plant Protection, 45, 20–27. (in Chinese)
Zhang X, Lan W, Deng Y, Ma Y, Liu K, Peng J, Li Y, Hong H. 2008. Highly passage of Spodoptera litura cell line caused its permissiveness to baculovirus infection. Cytotechnology, 57, 233–243.
Zheng G L, Li C Y, Zhou H X, Li S W, Li G X, Xue M. 2010. Establishment of two new cell lines from the embryonic tissue of Helicoverpa armigera (Lepidoptera: Noctuidae) and their responses to baculovirus infection. Acta Entomologica Sinica, 53, 167–174. (in Chinese)
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