Skip to main content
SpringerLink
Log in

Entomopathogenic Viruses in the Neotropics: Current Status and Recently Discovered Species

  • Forum
  • Published:
Neotropical Entomology Aims and scope Submit manuscript

Abstract

The market for biological control of insect pests in the world and in Brazil has grown in recent years due to the unwanted ecological and human health impacts of chemical insecticides. Therefore, research on biological control agents for pest management has also increased. For instance, insect viruses have been used to protect crops and forests around the world for decades. Among insect viruses, the baculoviruses are the most studied and used viral biocontrol agent. More than 700 species of insects have been found to be naturally infected by baculoviruses, with 90% isolated from lepidopteran insects. In this review, some basic aspects of baculovirus infection in vivo and in vitro infection, gene content, viral replication will be discussed. Furthermore, we provide examples of the use of insect viruses for biological pest control and recently characterized baculoviruses in Brazil.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig 1
Fig 2
Fig 3
Fig 4
Fig 5

Similar content being viewed by others

References

  • Aragão-Silva CW, Andrade MS, Ardisson-Araújo DMP, Fernandes JEA, Morgado FS, Báo SN, Moraes RHP, Wolff JLC, Melo FL, Ribeiro BM (2016) The complete genome of a baculovirus isolated from an insect of medical interest: Lonomia obliqua (Lepidoptera: Saturniidae). Sci Rep 6:23127

  • Ardisson-Araújo DMP, Melo FL, de Souza AM, Brancalhão RMC, Báo SN, Ribeiro BM (2014a) Complete genome sequence of the first non-Asian isolate of Bombyx mori nucleopolyhedrovirus. Virus Genes 49:477–484

    Article  PubMed  CAS  Google Scholar 

  • Ardisson-Araújo DMP, de Melo FL, de Souza AM, Sihler W, Báo SN, Ribeiro BM, de Souza ML (2014b) Genome sequence of Erinnyis ello granulovirus (ErelGV), a natural cassava hornworm pesticide and the first sequenced sphingid-infecting betabaculovirus. BMC Genomics 15:856

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ardisson-Araújo DMP, Sosa-Gómez DR, Melo FL, Báo SN, Ribeiro BM (2015) Characterization of Helicoverpa zea single nucleopolyhedrovirus isolated in Brazil during the first old world bollworm (Noctuidae: Helicoverpa armigera) nationwide outbreak. Virus Rev Res 20:1–4

    Article  Google Scholar 

  • Ardisson-Araújo DM, Lima RN, Melo FL, Clem RJ, Huang N, Báo SN, Sosa-Gómez DR, Ribeiro BM (2016a) Genome sequence of Perigonia lusca single nucleopolyhedrovirus: insights into the evolution of a nucleotide metabolism enzyme in the family Baculoviridae. Sci Rep 6:24612

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ardisson-Araújo DMP, Pereira BT, Melo FL, Ribeiro BM, Báo SN, Zanotto PMA, Kitajima EW, Sosa-Gómez DR, Wolff JL (2016b) A betabaculovirus encoding a gp64 homolog. BMCgenomics 17:94

    Google Scholar 

  • Ardisson-Araújo DM, Silva AMR, Melo FL, Santos ER, Sosa-Gómez DR, Ribeiro BM (2018) A novel betabaculovirus isolated from the monocot pest Mocis latipes (Lepidoptera: Noctuidae) and the evolution of multiple-copy genes. Viruses 10:134

    Article  PubMed Central  CAS  Google Scholar 

  • Arthurs S, Dara SK (2019) Microbial biopesticides for invertebrate pests and their markets in the United States. J Invertebr Pathol 165:13–21

    Article  PubMed  Google Scholar 

  • Beniya H, Funk CJ, Rohrmann GF, Weaver RF (1996) Purification of a virus-induced RNA polymerase from Autographa californica nuclear polyhedrosis virus-infected Spodoptera frugiperda cells that accurately initiates late and very late transcription in vitro. Virology 216:12–19

    Article  CAS  PubMed  Google Scholar 

  • Berling M, Blachere-Lopez C, Soubabere O, Lery X, Bonhomme A, Sauphanor B, Lopez-Ferber M (2009a) Cydia pomonella granulovirus genotypes overcome virus resistance in the codling moth and improve virus efficiency by selection against resistant hosts. Appl Environ Microbiol 75:925–930

    Article  CAS  PubMed  Google Scholar 

  • Berling M, Rey J-B, Ondet S-J, Tallot Y, Soubabere O, Bonhomme A, Sauphanor B, Lopez-Ferber M (2009b) Field trials of CpGV virus isolates overcoming resistance to CpGVM. Virol Sin 24:470–477

    Article  Google Scholar 

  • Bleckmann M, Fritz MH-Y, Bhuju S, Jarek M, Schurig M, Geffers R, Benes V, Besir H, van den Heuvel L (2015) Genomic analysis and isolation of RNA polymerase II dependent promoters from Spodoptera frugiperda. PLoS One 10:e0132898

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Blissard GW (1996) Baculovirus-insect cell interactions. Cytotechnology 20:73–93

    Article  CAS  PubMed  Google Scholar 

  • Boldogkői Z, Moldován N, Szűcs A, Tombácz D (2018) Transcriptome-wide analysis of a baculovirus using nanopore sequencing. Scientific Data 5:180276

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Boogaard B, Van Oers MM, Van Lent JWM (2018) An advanced view on baculovirus per Os infectivity factors. Insects 9:84

    Article  PubMed Central  Google Scholar 

  • Bovo S, Mazzoni G, Ribani A, Utzeri VJ, Bertolini F, Schiavo G, Fontanesi L (2017) A viral metagenomic approach on a non-metagenomic experiment: mining next generation sequencing datasets from pig DNA identified several porcine parvoviruses for a retrospective evaluation of viral infections. PLoS One 12:e0179462

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brand IL, Civciristov S, Taylor NL, Talbo GH, Pantaki-Eimany D, Levina V, Clem RJ, Perugini A, Kvansakul M, Hawkins CJ (2012) Caspase inhibitors of the P35 family are more active when purified from yeast than bacteria. PLoS One 7:e39248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Braunagel SC, Russell WK, Rosas-Acosta G, Russel DH, Summers MD (2003) Determination of the protein composition of the occlusion-derived virus of Autographa californica nucleopolyhedrovirus. Proc Natl Acad Sci 100:9797–9802

    Article  CAS  PubMed  Google Scholar 

  • Brito AFD, Braconi CT, Weidmann M, Dilcher M, Alves JMP, Gruber A, Zanotto PMA (2015) The pangenome of the Anticarsia gemmatalis multiple nucleopolyhedrovirus (AgMNPV). Genome Biol Evol 8:94–108

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brito AF, Melo FL, Ardisson-Araújo DMP, Sihler W, Souza ML, Ribeiro BM (2018) Genome-wide diversity in temporal and regional populations of the betabaculovirus Erinnyis ello granulovirus (ErelGV). BMC Genomics 19:698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buerger P, Hauxwell C, Murray D (2007) Nucleopolyhedrovirus introduction in Australia. Virol Sin 22:173–179

    Article  CAS  Google Scholar 

  • Byers NM, Vandergaast RL, Friesen PD (2015) Baculovirus inhibitor-of-apoptosis Op-IAP3 blocks apoptosis by interaction with and stabilization of a host insect cellular IAP. J Virol 90:533–544

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carballo A, Murillo R, Jakubowska A, Herrero S, Williams T, Caballero P (2017) Co-infection with iflaviruses influences the insecticidal properties of Spodoptera exigua multiple nucleopolyhedrovirus occlusion bodies: implications for the production and biosecurity of baculovirus insecticide. PLoS One 12:e0177301

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Castro MEB, Melo FL, Tagliari M, Inglis PW, Craveiro SR, Ribeiro ZMA, Ribeiro BM, Báo SN (2017) The genome sequence of Condylorrhiza vestigialis NPV, a novel baculovirus for the control of the Alamo Moth on Populus spp. in Brazil. J Invertebr Pathol 148:152–161

    Article  CAS  PubMed  Google Scholar 

  • Chen YP, Becnel JJ, Valles SM (2012) RNA viruses infecting pest insects. In: Vega FE, Kaya HK (eds) Insect pathology. Elsevier Science, Amsterdam, pp 133–170

    Chapter  Google Scholar 

  • Chen Y-R, Zhong S, Fei Z, Hashimoto Y, Xiang JZ, Zhang S, Blissard GW (2013) The transcriptome of the baculovirus Autographa californica multiple nucleopolyhedrovirus in Trichoplusia ni cells. J Virol 87:6391–6405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y-R, Zhong S, Fei Z, Gao S, Zhang S, Li Z, Wang P, Blissard GW (2014) Transcriptome responses of the host Trichoplusia ni to infection by the Baculovirus Autographa californica multiple nucleopolyhedrovirus. J Virol 88:13781–13797

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Choi JY, Roh JY, Wang Y, Zhen Z, Tao XY, Lee JH, Liu Q, Kim JS, Shin SW, Je YH (2012) Analysis of genes expression of Spodoptera exigua larvae upon AcMNPV infection. PLoS One 7:e42462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clem RJ, Passarelli AL (2013) Baculoviruses: sophisticated pathogens of insects. PLoS Pathog 9:e1003729

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Craveiro SR, Inglis PW, Togawa RC, Grynberg P, Melo FL, Ribeiro ZMA, Ribeiro BM, Bao SN, Castro MEB (2015) The genome sequence of Pseudoplusia includens single nucleopolyhedrovirus and an analysis of p26 gene evolution in the baculoviruses. BMC Genomics 16:127

    Article  PubMed  PubMed Central  Google Scholar 

  • Cuartas PE, Villamizar LF, Barrera GP, Ruiz JC, Campos JC, León-Martínez G, Gómez Valderrama J (2019) Novel biopesticide based on Erinnyis ello betabaculovirus: characterization and preliminary field evaluation to control Erinnyis ello in rubber plantations. Pest Manag Sci 75:1391–1399

    Article  CAS  PubMed  Google Scholar 

  • Deeks S, Drosten C, Picker L, Subbara K, Suzich J (2013) Roadblocks to translational challenges on viral pathogenesis. Nat Med 19:30–34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delwart E (2012) Animal virus discovery: improving animal health, understanding zoonoses, and opportunities for vaccine development. Curr Opin Virol 2:344–352

    Article  PubMed  PubMed Central  Google Scholar 

  • Donly BC, Theilmann DA, Hegedus DD, Dwayne DB, Bldwin D, Ealandson MA (2014) Mamestra configurata nucleopolyhedrovirus-a transcriptome from infected host midgut. Virus Genes 48:174–183

    Article  CAS  PubMed  Google Scholar 

  • dos Santos ER, Trentin LB, Ecker A, Silva LA, Borges M, Mowery JD, Ribeiro BM, Harrison RL, Ardisson-Araújo DM (2019) An iflavirus found in stink bugs (Hemiptera: Pentatomidae) of four different species. Virology 534:72–79

    Article  PubMed  CAS  Google Scholar 

  • Engelhard EK, Kam-Morgan LN, Washburn JO, Volkman LE (1994) The insect tracheal system: a conduit for the systemic spread of Autographa californica M nuclear polyhedrosis virus. Proc Natl Acad Sci 91:3224–3227

    Article  CAS  PubMed  Google Scholar 

  • Federici BA (1986) Ultrastructure of baculoviruses. In: Granados RR, Federici BA (eds) The biology of baculoviruses. CRC Press, Boca Raton, pp 61–88

    Google Scholar 

  • François S, Filloux D, Roumagnac P, Bigot D, Gayral P, Martin DP, Froissart R, Oliastro M (2016) Discovery of parvovirus-related sequences in an unexpected broad range of animals. Sci Rep 6:30880

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Friesen PD (1997) Regulation of baculovírus early gene expression. In: Miller LK (ed) The baculoviruses. Plenum Press, New York, pp 7–32

    Google Scholar 

  • Fritsch E, Undorf-Spahn K, Kienzle J, Zebitz CPW, Huber J (2005) Apfelwickler-Granulovirus: Erste Hinweise auf Unterschiede in der Empfindlichkeit lokaler Apfelwickler-Populationen. Nachrichtenbl Dtsch Pflanzenschutzdienst 57:29–34

    Google Scholar 

  • Glocker B, Hoopes RR, Rohrmann GF (1992) In vitro transactivation of baculovirus early genes by nuclear extracts from Autographa californica nuclear polyhedrosis virus infected Spodoptera frugiperda cells. J Virol 66:3476–3484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glocker B, Hoopes RR, Hodges L, Rohrmann GF (1993) In vitro transcription from baculovirus late gene promoters: accurate mRNA initiation by nuclear extracts prepared from infected Spodoptera frugiperda cells. J Virol 67:3771–3776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Granados RR, Lawler KA (1981) In vivo pathway of Autographa californica baculovirus invasion and infection. Virology 108:297–308

    Article  CAS  PubMed  Google Scholar 

  • Granados RR, Williams KA (1986) In vivo infection and replication of baculoviruses. In: Granados RR, Federici BA (eds) The biology of baculoviruses. CRC Press, Boca Raton, pp 89–108

    Google Scholar 

  • Grzywacz D, Jones K, Moawad G, Cherry J (1998) The in vivo production of Spodoptera littoralis nuclear polyhedrosis virus. J Virol Methods 71:115–122

    Article  CAS  PubMed  Google Scholar 

  • Guarino LA, Smith M (1992) Regulation of delayed-early gene transcription by dual TATA boxes. J Virol 66:3733–3739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guarino LA, Xu B, Jin J, Dong W (1998) A virus-encoded RNA polymerase purified from baculovirus-infected cells. J Virol 72:7985–7991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haase S, Sciocco-Cap A, Romanowski V (2015) Baculovirus insecticides in Latin America: historical overview, current status and future perspectives. Viruses 7:2230–2267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hajek AE, van Franknhuyzen K (2017) Use of entomopathogens against forest pests. In: Lacey L (ed) Microbial control of insect and mite pests. From theory to practice. Academic Press Elsevier, Amsterdan, pp 313–330

    Chapter  Google Scholar 

  • Harrison R, Herniou E, Jehle J, Theilmann D, Burand J, Becnel J, Krell P, van Oers M, Mowery J, Bauchan G (2018) ICTV report consortium. J Gen Virol 99:1185–1186

    Article  CAS  PubMed  Google Scholar 

  • Hatting JL, Moore SD, Malan AP (2018) Microbial control of phytophagous invertebrate pests in South Africa: current status and future prospects. J Invertebr Pathol 165:54–66

    Article  PubMed  Google Scholar 

  • Hawtin RE, Zarkowska T, Arnold K, Thomas CJ, Gooday GW, King LA, Kuzio JA, Possee RD (1997) Liquefaction of Autographa californica nucleopolyhedrovirus infected insects is dependent on the integrity of virus encoded chitinase and cathepsin genes. Virology 238:243–253

    Article  CAS  PubMed  Google Scholar 

  • Hayakawa T, Rohrmann GF, Hashimoto Y (2000) Patterns of genome organization and content in lepidopteran baculoviruses. Virology 278:1–12

    Article  CAS  PubMed  Google Scholar 

  • Hefferon KL, Oomens AGP, Monsma SA, Finnerty CM, Blissard GW (1999) Host cell receptor binding by baculovirus GP64 and kinetics of virion entry. Virology 258:455–468

    Article  CAS  PubMed  Google Scholar 

  • Herniou EA, Luque T, Chen X, Vlak JM, Winstanley D, Cory JS, O’Reilly D (2001) Use of whole genome sequence data to infer baculovirus phylogeny. J Virol 75:8117–8126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herniou EA, Olszewski JA, Cory JS, O'Reilly DR (2003) The genome sequence and evolution of baculoviruses. Annu Rev Entomol 48:211–234

    Article  CAS  PubMed  Google Scholar 

  • Hodgson JJ, Buchon N, Blissard GW (2019) Identification of insect genes involved in baculovirus AcMNPV entry into insect cells. Virology 527:1–11

    Article  CAS  PubMed  Google Scholar 

  • Iwanaga M, Takaya K, Katsuma S, Ote M, Tanaka S, Kamita SG, Kang W, Shimada T, Kobayashi M (2004) Expression profiling of baculovirus genes in permissive and nonpermissive cell lines. Biochem Biophys Res Commun 323:599–614

    Article  CAS  PubMed  Google Scholar 

  • Javed MA, Biswas S, Willis LG, Harris S, Pritchard C, Van Oers MM, Donly BC, Erlandson MA, Hegedus DD, Theilmann DA (2017) Autographa californica multiple nucleopolyhedrovirus AC83 is a per os infectivity factor (PIF) protein required for occlusion-derived virus (ODV) and budded virus nucleocapsid assembly as well as assembly of the P IF complex in ODV envelopes. J Virol 91:e02115–e02116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jehle JA, Blissard GW, Bonning BC, Cory JS, Heniou EA, Rhormann GF, Theilmann DA, Thiem SM, Vlak JM (2006) On the classification and nomenclature of baculoviruses: a proposal for revision. Arch Virol 151:1257–1266

    Article  CAS  PubMed  Google Scholar 

  • Junglen S, Drosten C (2013) Virus discovery and recent insights into virus diversity in arthropods. Curr Opin Microbiol 16:507–513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamita SG, Nagasaka K, Chua J, Mita YSK, Kobayashi M, Maeda S, Hammock BD (2005) A baculovirus-encoded protein tyrosine phosphatase gene induces enhanced locomotory activity in a lepidopteran host. Proc Natl Acad Sci 102:2584–2589

    Article  CAS  PubMed  Google Scholar 

  • Katsuma S, Koyano Y, Kang W, Kokusho R, Kamita SG, Shimada T (2012) The baculovirus uses a captured host phosphatase to induce enhanced locomotory activity in host caterpillars. PLoS Pathog 8:e1002644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawasaki Y, Matsumoto S, Nagamine T (2004) Analysis of baculovirus IE1 in living cells: dynamics and spatial relationships to viral structural proteins. J Gen Virol 85:3575–3583

    Article  CAS  PubMed  Google Scholar 

  • Kogan PH, Blissard GW (1994) A baculovirus gp64 early promoter is activated by host transcription factor binding to CACGTG and GATA elements. J Virol 68:813–822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kool M, Ahrens CH, Goldbach RW, Rohrmann GF, Vlak JM (1994) Identification of genes involved in DNA replication of the Autographa californica baculovirus. Proc Natl Acad Sci 91:11212–11216

    Article  CAS  Google Scholar 

  • Kumar KK, Sridhar J, Murali-Baskaran RK, Senthil-Nathan S, Kaushal P, Dara SK, Arthurs S (2019) Microbial biopesticides for insect pest management in India: current status and future prospects. J Invertebr Pathol 165:74–81

    Article  CAS  PubMed  Google Scholar 

  • Kunimi Y (2007) Current status and prospects on microbial control in Japan. J Invertebr Pathol 95:181–186

    Article  PubMed  Google Scholar 

  • Lacey J (2017) Microbial control of insect and mite pests. From theory to practice. Academic Press Elsevier, Amsterdan p461

    Google Scholar 

  • Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M, Goettel MS (2015) Insect pathogens as biological control agents: back to the future. J Invertebr Pathol 132:1–41

    Article  CAS  PubMed  Google Scholar 

  • Lima AA, Aragão CWS, Castro MEB, Oliveira JVC, Sosa-Gómez DR, Ribeiro BM (2013) A recombinant Anticarsia gemmatalis MNPV harboring chiA and v-cath genes from Choristoneura fumiferana defective NPV induce host liquefaction and increased insecticidal activity. PLoS One 8:e74592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu S, Vijayendran D, Bonning BC (2011a) Next generation sequencing technologies for insect virus discovery. Viruses 3:1849–1869

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu XY, Ma XH, Lei CF, Xiao YZ, Zhang ZX, Sun XL (2011b) Synergistic effects of Cydia pomonella granulovirus GP37 on the infectivity of nucleopolyhedroviruses and the lethality of Bacillus thuringiensis. Arch Virol 156:1707–1715

    Article  CAS  PubMed  Google Scholar 

  • Long G, Pan X, Kormelink R, Vlak JM (2006) Functional entry of baculovirus into insect and mammalian cells is dependent on clathrin-mediated endocytosis. J Virol 80:8830–8833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu A, Carstens EB (1993) Immediate-early baculovirus genes transactivate the p143 gene promoter of Autographa californica nuclear polyhedrosis virus. Virology 195:710–718

    Article  CAS  PubMed  Google Scholar 

  • Lu A, Miller LK (1995a) Differential requirements for baculovirus late expression factor genes in two cell lines. J Virol 69:6265–6272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu A, Miller LK (1995b) The roles of eighteen baculovirus late expression factor genes in transcription and DNA replication. J Virol 69:975–982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu A, Miller LK (1997) Regulation of baculovirus late and very late gene expression. In: Miller LK (ed) The baculoviruses. Plenum Press, New York, pp 193–216

    Chapter  Google Scholar 

  • Lucena CC, Silveira HF, Ringenberg R, Rangel MAS (2017) Diagnóstico da situação atual do manejo de artrópodes e pragas na cultura da mandioca na região Centro-Sul do Brasil. Boletim de Pesquisa e Desenvolvimento, Embrapa Mandioca e Fruticultura:35 p

  • Machado EB, Sousa NJ, Moscardi F (2017) Eficiência em campo de diferentes concentrações de Condylorrhiza vestigiais multiple nucleopolyhedrovirus no controle de Condylorrhiza vestigiais. Rev Flore 47:207–212

    Article  Google Scholar 

  • Maori E, Paldi N, Shafir S, Kalev H, Tsur E, Glick E, Sela I (2009) IAPV, a bee-affecting virus associated with colony collapse disorder can be silenced by dsRNA ingestion. Insect Mol Biol 18:55–60

    Article  CAS  PubMed  Google Scholar 

  • McTaggart SJ, Hannah T, Bridgett S, Garbutt JS, Kaur G, Boots M (2015) Novel insights into the insect trancriptome response to a natural DNA virus. BMC Genomics 16:310

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Means JC, Passarelli AL (2010) Viral fibroblast growth factor, matrix metalloproteases, and caspases are associated with enhancing systemic infection by baculoviruses. Proc Natl Acad Sci 107:9825–9830

    Article  CAS  PubMed  Google Scholar 

  • Mehrabadi M, Hussain M, Matindoost L, Asgari S (2015) The baculovirus antiapoptotic p35 protein functions as an inhibitor of the host RNA interference antiviral response. J Virol 89:8182–8192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mensah RK, Liang W, Gibb D, Coates R, Johnson D (2005) Improving the efficacy of nuclear polyhedrosis virus and Bacillus thuringiensis against Helicoverpa spp. with ultra-violet light protected petroleum spray oils on cotton crops in Australia. Int J Pest Manag 51:101–109

    Article  Google Scholar 

  • Moldován N, Tombácz D, Szűcs A, Csabai Z, Balázs Z, Kis E, Monár J, Boldogkói Z (2018) Third-generation sequencing reveals extensive polycistronism and transcriptional overlapping in a baculovirus. Sci Rep 8:8604

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Morgado F, Ardisson-Araújo D, Ribeiro B (2017) Real-time expression analysis of selected Anticarsia gemmatalis multiple nucleopolyhedrovirus gene promoters during infection of permissive, semipermissive and nonpermissive cell lines. Viruses 9:132

    Article  PubMed Central  CAS  Google Scholar 

  • Moscardi F (1999) Assessment of the application of baculoviruses for control of Lepidoptera. Annu Rev Entomol 44:257–289

    Article  CAS  PubMed  Google Scholar 

  • Moscardi F, Sosa-Gómez DR (1992) Use of viruses against soybean caterpillars in Brazil. In: Copping LG, Green MB, Rees RT (eds) Pest Management in Soybean. Springer, Dordrecht, pp 98–109

    Chapter  Google Scholar 

  • Moscardi F, Souza ML, Castro MEB, Moscardi ML, Szewczyk B (2011) Baculovirus pesticides: present state and future perspectives. In: Ahmad I, Ahmad F, Pichtel J (eds) Microbes and microbial technology. Springer, New York, pp 415–445

    Chapter  Google Scholar 

  • Murphy FA, Fauquet CM, Bishop DHL, Ghabrial SA, Jarvis AW, Martelli GP, Mayo MA, Summers MD (eds) (1995) Virus taxonomy – the classification and nomenclature of viruses: sixth report of the international committee on taxonomy of viruses. Springer-Verlag, NewYork

    Google Scholar 

  • Nagamine T, Kawasaki Y, Iizuka T, Matsumoto S (2005) Focal distribution of baculovirus IE1 triggered by its binding to the hr DNA elements. J Virol 79:39–46

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagamine T, Kawasaki Y, Matsumoto S (2006) Induction of a subnuclear structure by the simultaneous expression of baculovirus proteins, IE1, LEF3, and P143 in the presence of hr. Virology 352:400–407

    Article  CAS  PubMed  Google Scholar 

  • Nguyen Q, Palfreyman RW, Chan LCL, Reid S, Nielsen LK (2012) Transcriptome sequencing of and microarray development for a Helicoverpa zea cell line to investigate in vitro insect cell baculovirus interactions. PLoS One 7:e36324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen Q, Chan LCL, Nielsen LK, Reid S (2013) Genome scale analysis of differential mRNA expression of Helicoverpa zea insect cells infected with a H. armigera baculovirus. Virology 444:158–170

    Article  CAS  PubMed  Google Scholar 

  • O’Reilly DR (1997) Auxiliary genes of baculoviruses. In: Miller LK (ed) The baculoviruses. Plenum Press, New York, pp 267–300

    Chapter  Google Scholar 

  • Ohkawa T, Welch MD (2018) Baculovirus actin-based motility drives nuclear envelope disruption and nuclear egress. Curr Biol 28:2153–2159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohresser M, Morin N, Cerutti M, Delsert C (1994) Temporal regulation of a complex and unconventional promoter by viral products. J Virol 68:2589–2597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliveira JDC, Wolff JLC, Garcia-Maruniak A, Ribeiro BM, Castro MEB, Souza ML, Moscardi F, Maruniak JE, Zanotto PMA (2006) Genome of the most widely used viral biopesticide: Anticarsia gemmatalis multiple nucleopolyhedrovirus. J Gen Virol 87:3233–3250

    Article  CAS  PubMed  Google Scholar 

  • Ooi BG, Miller LK (1988) Regulation of host RNA levels during baculovirus infection. Virology 166:515–523

    Article  CAS  PubMed  Google Scholar 

  • Pearson MN, Groten C, Rohrmann GF (2000) Identification of the Lymantria dispar nucleopolyhedrovirus envelope fusion protein provides evidence for a phylogenetic division of the Baculoviridae. J Virol 74:6126–6131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng K, van Lent JW, Boeren S, Fang M, Theilmann DA, Erlandson MA, Vlak JM, van Oers MM (2012) Characterization of novel components of the baculovirus per os infectivity factor complex. J Virol 86:4981–4988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pennock GD, Shoemaker C, Miller LK (1984) Strong and regulated expression of Escherichia coli beta-galactosidase in insect cells with a baculovirus vector. Mol Cell Biol 4:399–406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pombo V, Velloso L, Ribeiro BM, Bao SN (1998) Structural and ultrastructural changes during the infection of UFL-AG-286 cells with the baculovirus AgMNPV. J Invertebr Pathol 72:239–245

    Article  CAS  PubMed  Google Scholar 

  • Pullen SS, Friesen PD (1995a) Early transcription of the ie-1 transregulator gene of Autographa californica nuclear polyhedrosis virus is regulated by DNA sequences within its 5′ noncoding leader region. J Virol 69:156–165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pullen SS, Friesen PD (1995b) The CAGT motif functions as an initiator element duringearly transcription of the baculovirus transregulator ie-1. J Virol 69:3575–3583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramírez-Arias FG, Lasa R, Murillo R, Navarro-de-la-Fuente L, Mercado G, Williams T (2019) Post-mortem incubation influences occlusion body production in nucleopolyhedrovirus-infected larvae of Spodoptera frugiperda. Biol Control 135:33–40

    Article  Google Scholar 

  • Rapp JC, Wilson JA, Miller LK (1998) Nineteen baculovirus open reading frames, including LEF-12, support late gene expression. J Virol 72:10197–101206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Redman EM, Wilson K, Grzywacs D, Cory JS (2010) High levels of genetic diversity in Spodoptera exempta NPV from Tanzania. J Invertebr Pathol 105:190–193

    Article  PubMed  Google Scholar 

  • Ribeiro BM, Hutchinson K, Miller LK (1994) A mutant baculovirus with a temperature sensitive IE-1 transregulatory protein. J Virol 68:1075–1084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ribeiro BM, Santos ER, Trentin LB, Silva LA, Melo FL, Kitajima EW, Ardisson-Araújo DMP (2019) A Nymphalid-infecting group I alphabaculovirus isolated from the major passion fruit caterpillar pest Dione juno juno (Lepidoptera: Nymphalidae). Viruses 11:602

  • Rice WC, Miller LK (1986) Baculovirus transcription in the presence of inhibitors and in nonpermissive Drosophila cells. Virus Res 6:155–172

    Article  CAS  PubMed  Google Scholar 

  • Rodems SM, Pullen SS, Friesen PD (1997) DNA-dependent transregulation by IE1 of Autographa californica nuclear polyhedrosis virus: IE1 domains required for transactivation and DNA binding. J Virol 71:9270–9277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodrigues JC, De Souza ML, O’Reilly D, Velloso LM, Pinedo FJR, Razuck FB, Ribeiro B, Ribeiro BM (2001) Characterization of the ecdysteroid UDP-glucosyltransferase (egt) gene of Anticarsia gemmatalis nucleopolyhedrovirus. Virus Genes 22:103–112

    Article  CAS  PubMed  Google Scholar 

  • Rohrmann GF (2019). Baculovirus Molecular Biology. 4th edition. Bethesda (MD): National Center for Biotechnology Information (US) https://www.ncbi.nlm.nih.gov/books/NBK543458/

  • Roossinck MJ (2011) The good viruses: viral mutualistic symbioses. Nat Rev Microbiol 9:99–108

    Article  CAS  PubMed  Google Scholar 

  • Ros VID, van Houte S, Hemerik L, Van Oers MM (2014) Baculovirus-induced tree-top disease: how extended is the role of egt as a gene for the extended phenotype? Mol Ecol 24:249–258

    Article  PubMed  CAS  Google Scholar 

  • Ruiz C, Gómez-Valderrama J, Chaparro M, Sotelo P, Villamizar L (2015) Adjusting the conditions of a system for the in vivo production of a nucleopolyhedrovirus of Spodoptera frugiperda (Lepidoptera: Noctuidae). Biotecnol Apl 32:4311–4316

    Google Scholar 

  • Ryabov EV, Keane G, Naish N, Evered C, Winstanley D (2009) Densovirus induces winged morphs in asexual clones of the rosy apple aphid, Dysaphis plantaginea. Proc Natl Acad Sci 106:8465–8470

    Article  CAS  Google Scholar 

  • Sajjadian M, Hosseininaveh V (2015) Destruction of peritrophic membrane and its effect on biological characteristics and activity of digestive enzymes in larvae of the Indian meal moth, Plodia interpunctella (Lepidoptera: Pyralidae). Eur J Entomol 112:245–250

  • Salem TZ, Zhang F, Xie Y, Thiem SM (2011) Comprehensive analysis of host gene expression in Autographa californica nucleopolyhedrovirus-infected Spodoptera frugiperda cells. Virology 412:167–178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santos ER, Oliveira LB, Peterson L, Sosa-Gómez DR, Ribeiro BM, Ardisson-Araújo DM (2018) The complete genome sequence of the first hesperiid-infecting alphabaculovirus isolated from the leguminous pest Urbanus proteus (Lepidoptera: Hesperiidae). Virus Res 249:76–84

    Article  CAS  PubMed  Google Scholar 

  • Sauer AJ, Schulze-Bopp S, Fritsch E, Undorf-Spahn K, Jehle JA (2017) A third type of resistance to Cydia pomonella granulovirus in codling moths shows a mixed Z-linked and autosomal inheritance pattern. Appl Environ Microbiol 83:e01036–e01017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saxena A, Byram P, Singh CJ, Murhammer D, Giri L (2018) A structured review of baculovirus infection process: integration of mathematical models and biomolecular information on cell–virus interaction. J Gen Virol 99:1151–1171

    Article  CAS  PubMed  Google Scholar 

  • Schmidt O, Theopold U, Strand M (2001) Innate immunity and its evasion and suppression by hymenopteran endoparasitoids. BioEssays 23:344–351

    Article  CAS  PubMed  Google Scholar 

  • Schmitt AT (1985) Eficiência da aplicação de Baculovirus erinnyis no controle do mandarová da mandioca. Florianópolis: Empasc, Comunicado Técnico 88:7p

  • Schmitt AT (1986) Aplicação de Baculovirus erinnyis no controle do mandarová-da-mandioca. In: IV Congresso Brasileiro de Mandioca. Resumos, Brasil, Camboriú, p 11

    Google Scholar 

  • Schmitt A, Bisutti IL, Ladurner E, Benuzzi M, Sauphanor B, Kienzle J, Zingg D, Undorf-Spahn K, Fritsch E, Huber J, Jehle JA (2013) The occurrence and distribution of resistance of codling moth to Cydia pomonella granulovirus in Europe. J Appl Entomol 137:641–649

    Article  Google Scholar 

  • Shi M, Lin X, Tian J, Chen L, Chen X, Li C, Qin X, Li J, Cao J, Eden J, Buchmann J, Wang W, Xu J, Holmes EC, Zhang Y (2016) Redefining the invertebrate RNA virosphere. Nature 540:539–543. https://doi.org/10.1038/nature20167

    Article  CAS  PubMed  Google Scholar 

  • Shrestha A, Bao K, Chen Y-R, Chen W, Wang P, Fei Z, Blissard GW (2018) Global analysis of Baculovirus Autographa californica multiple nucleopolyhedrovirus gene expression in the Midgut of the Lepidopteran host Trichoplusia ni. J Virol 92:e01277–e01218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shrestha A, Bao K, Chen W, Wang P, Fei Z, Blissard GW (2019) Transcriptional responses of the Trichoplusia ni midgut to oral infection by the baculovirus Autographa californica multiple nucleopolyhedrovirus. J Virol 93:e00353–e00319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silva LA, Ardisson-Araujo DMP, Tinocco RS, Fernandes OA, Melo FL, Ribeiro BM (2015) Complete genome sequence and structural characterization of a novel iflavirus isolated from Opsiphanes invirae (Lepidoptera: Nymphalidae). J Invertebr Pathol 130:136–140

    Article  CAS  PubMed  Google Scholar 

  • Singh CP, Singh J, Nagaraju J (2014) Bmnpv-miR-3 facilitates BmNPV infection by modulating the expression of viral P6.9 and other late genes in Bombyx mori. Insect Biochem Mol Biol 49:59–69

    Article  CAS  PubMed  Google Scholar 

  • Slack JM, Ribeiro BM, de Souza ML (2004) The gp64 locus of Anticarsia gemmatalis multicapsid nucleopolyhedrovirus contains a 3′ repair exonuclease homologue and lacks v-cath and ChiA genes. J Gen Virol 85:211–219

    Article  CAS  PubMed  Google Scholar 

  • Sosa-Gómez DR (2017) Microbial control of soybean pest insects and mites. In: Lacey L (ed) Microbial control of insect and mite pests. From theory to practice. Academic Press Elsevier, Amsterdam, pp 199–208

    Chapter  Google Scholar 

  • Sosa-Gómez DR, Kitajima EW, Rolón M (1994) First record of entomopathogenic diseases in Paraguay tea agroecosystem in Argentina. Fla Entomol 77:378–382

    Article  Google Scholar 

  • Sosa-Gómez DR, Moscardi F, Santos B, Alves LFA, Alves SB (2008) Produção e uso de vírus para o controle de pragas na América Latina. In: Alves, Sérgio Batista & Lopes, Rogério Biaggioni. (Org.). Controle Microbiano de pragas na América Latina: Avanços e Desafios. 1 ed. FEALQ, Piracicaba, pp 49–68

  • Srinivasan R, Sevgan S, Ekesi S, Tamò M (2019) Biopesticide based sustainable pest management for safer production of vegetable legumes and brassicas in Asia and Africa. Pest Manag Sci 75:2446–2454

    CAS  PubMed  Google Scholar 

  • Sugiura N, Ikeda M, Shioiri T, Yoshimura M, Kobayashi M, Watanabe H (2013) Chondroitinase from baculovirus Bombyx mori nucleopolyhedrovirus and chondroitin sulfate from silkworm Bombyx mori. Glycobiology 23:1520–1530

    Article  CAS  PubMed  Google Scholar 

  • Sun L, Liu P, Sun S, Yan S, Cao C (2019) Transcriptomic analysis of interactions between Hyphantria cunea larvae and nucleopolyhedrovirus. Pest Manag Sci 75:1024–1033

    Article  CAS  PubMed  Google Scholar 

  • Suttle C (2005) The viriosphere: the greatest biological diversity on earth and driver of global processes. Environ Microbiol 7:481–482

    Article  PubMed  Google Scholar 

  • Suttle CA (2007) Marine viruses - major players in the global ecosystem. Nat Rev Microbiol 5:801–812

    Article  CAS  PubMed  Google Scholar 

  • Thézé J, Takatsuka J, Nakai M, Arif B, Herniou E (2015) Gene acquisition convergence between entomopoxviruses and baculoviruses. Viruses 7:1960–1974

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Todd JW, Passarelli AL, Miller LK (1995) Eighteen baculovirus genes, including lef-11, p35, 39K, and p47, support late gene expression. J Virol 69:968–974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Todd JW, Passarelli AL, Lu A, Miller LK (1996) Factors regulating baculovirus late and very late gene expression in transient-expression assays. J Virol 70:2307–2317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trentin LB, Santos ER, Junior AGO, Sosa-Gómez DR, Ribeiro BM, Ardisson-Araújo DM (2019) The complete genome of Rachiplusia nu nucleopolyhedrovirus (RanuNPV) and the identification of a baculoviral CPD-photolyase homolog. Virology 534:64–71

    Article  CAS  PubMed  Google Scholar 

  • van Houte S, Ros VI, Mastenbroek TG, Vendrig NJ, Hoover K, Spitzen J, van Oers MM (2012) Protein tyrosine phosphatase-induced hyperactivity is a conserved strategy of a subset of baculoviruses to manipulate lepidopteran host behavior. PLoS One 7:e46933

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • van Oers MM, Vlak JM (2007) Baculovirus genomics. Curr Drug Targets 8:1051–1068

    Article  PubMed  Google Scholar 

  • van Oers MM, Pijlman GP, Vlak JM (2015) Thirty years of baculovirus-insect cell protein expression: from dark horse to mainstream technology. J Gen Virol 96:6–23

    Article  PubMed  CAS  Google Scholar 

  • Vieira CM, Tuelher ES, Valicente FH, Caldas-Wolff JL (2012) Characterization of a Spodoptera frugiperda multiple nucleopolyhedrovirus isolate that does not liquefy the integument of infected larvae. J Invertebr Pathol 111:189–192

    Article  CAS  PubMed  Google Scholar 

  • Volkman LE, Keddie BA (1990) Nuclear polyhedrosis virus pathogenesis. Semin Virol 1:249–256

    Google Scholar 

  • Wang P, Granados RR (1997) An intestinal mucin is the target substrate for a baculovirus enhancin. Proc Natl Acad Sci 94:6977–6982

    Article  CAS  PubMed  Google Scholar 

  • Wang M, Hu Z (2019) Cross-talking between baculoviruses and host insects towards a successful infection. Philos Trans R Soc B 374:20180324

    Article  CAS  Google Scholar 

  • Wang R, Deng F, Hou D, Zhao Y, Guo L, Wang H, Hu Z (2010) Proteomics of the Autographa californica nucleopolyhedrovirus budded virions. J Virol 84:7233–7242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Chen C, Zhang N, Li J, Deng F, Wang H, Vlak JM, Hu Z, Wang M (2018) The group I alphabaculovirus-specific protein, ac5, is a novel component of the occlusion body but is not associated with odvs or the pif complex. J Gen Virol 99:585–595

    Article  CAS  PubMed  Google Scholar 

  • Westenberg M, Uijtdewilligen P, Vlak J (2007) Baculovirus envelope fusion proteins F and GP64 exploit distinct receptors to gain entry into cultured insect cells. J Gen Virol 88:3302–3306

    Article  CAS  PubMed  Google Scholar 

  • Wickham TJ, Shuler ML, Hammer DA, Granados RR, Wood HA (1992) Equilibrium and kinetic analysis of Autographa californica nuclear polyhedrosis virus attachment to different insect cell lines. J Gen Virol 73:3185–3194

    Article  CAS  PubMed  Google Scholar 

  • Williams T, Virto C, Murillo R, Caballero P (2017) Covert infection of insects by Baculoviruses. Front Microbiol 8:1337

    Article  PubMed  PubMed Central  Google Scholar 

  • Wolff JL, Valicente FH, Martins R, Oliveira JVC, Zanotto PMA (2008) Analysis of the genome of Spodoptera frugiperda nucleopolyhedrovirus (SfMNPV-19) and of the high genomic heterogeneity in group II nucleopolyhedroviruses. J Gen Virol 89:1202–1211

    Article  CAS  PubMed  Google Scholar 

  • Xu B, Yoo S, Guarino LA (1995) Differential transcription of baculovirus late and very late promoters: fractionation of nuclear extracts by phosphocellulose chromatography. J Virol 69:2912–2917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xue J, Qiao N, Zhang W, Cheng R-L, Zhang X-Q, Bao Y-Y, Xu Y-P, Gu L-Z, Han JDJ, Zhang C-X (2012) Dynamic interactions between Bombyx mori nucleopolyhedrovirus and its host cells revealed by transcriptome analysis. J Virol 86:7345–7359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang CL, Stetler DA, Weaver RF (1991) Structural comparison of the Autographa californica nuclear polyhedrosis virus-induced RNA polymerase and the three nuclear RNA polymerases from the host, Spodoptera frugiperda. Virus Res 20:251–264

    Article  CAS  PubMed  Google Scholar 

  • Yuan C, Xing L, Wang M, Wang X, Yin M, Wang Q, Hu Z, Zou Z (2017) Inhibition of melanization by serpin-5 and serpin-9 promotes baculovirus infection in cotton bollworm Helicoverpa armigera. PLoS Pathog 13:e1006645

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zanotto PMA, Kessing BD, Maruniak JE (1993) Phylogenetic interrelationships among baculoviruses: evolutionary rates and host associations. J Invertebr Pathol 62:147–164

    Article  CAS  PubMed  Google Scholar 

  • Zeddam JL, Arroyo Cruzado J, Rodriguez JL, Ravallec M (2003) A new nucleopolyhedrovirus from the oil-palm leaf-eater Euprosterna elaeasa (Lepidoptera: Limacodidae): preliminary characterization and field assessment in Peruvian plantation. Agric Ecosyst Environ 96:69–75

    Article  Google Scholar 

  • Zhu M, Wang J, Deng R, Xiong P, Liang H, Wang X (2013) A MicroRNA encoded by Autographa californica Nucleopolyhedrovirus regulates expression of viral gene ODV E25. J Virol 87:13029–13034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu M, Wang J, Deng R, Wang X (2016) Functional regulation of an Autographa californica Nucleopolyhedrovirus-encoded MicroRNA, AcMNPV-miR-1, in Baculovirus replication. J Virol 90:6526–6537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Empresa Brasileira de Pesquisa Agropecuária, Embrapa Soja, Londrina, PR, Brasil

    D R Sosa-Gómez

  2. Depto de Biologia Celular, Univ of Brasília, Brasília, DF, Brasil

    F S Morgado, L A Silva, B M P Rodrigues & B M Ribeiro

  3. Depto de Biotecnologia, Univ Federal de Tocantins, Gurupi, TO, Brasil

    R F T Corrêa & R W S Aguiar

  4. Depto de Bioquímica e Biologia Molecular, Univ Federal de Santa Maria, Santa Maria, RS, Brasil

    D M P Ardisson-Araújo

  5. Depto de Entomologia, Univ Federal de Viçosa, Viçosa, MG, Brasil

    E E Oliveira

Authors
  1. D R Sosa-Gómez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F S Morgado
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R F T Corrêa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. L A Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. D M P Ardisson-Araújo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. B M P Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. E E Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. R W S Aguiar
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. B M Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to B M Ribeiro.

Additional information

Edited by Lessando Moreira Gontijo – UFV

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sosa-Gómez, D.R., Morgado, F.S., Corrêa, R.F.T. et al. Entomopathogenic Viruses in the Neotropics: Current Status and Recently Discovered Species. Neotrop Entomol 49, 315–331 (2020). https://doi.org/10.1007/s13744-020-00770-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13744-020-00770-1

Keywords

Search

Navigation