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

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, access via your institution.

Fig 1
Fig 2
Fig 3
Fig 4
Fig 5

References

  1. 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

  2. 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

    PubMed  Article  CAS  Google Scholar 

  3. 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  4. 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 

  5. 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  6. 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 

  7. 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

    PubMed Central  Article  CAS  Google Scholar 

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

    PubMed  Article  Google Scholar 

  9. 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

    CAS  PubMed  Article  Google Scholar 

  10. 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

    CAS  PubMed  Article  Google Scholar 

  11. 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 

  12. 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

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

    PubMed Central  Article  Google Scholar 

  16. 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  17. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  18. 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

    CAS  PubMed  Article  Google Scholar 

  19. 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  20. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  22. 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  23. 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  24. 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

    CAS  PubMed  Article  Google Scholar 

  25. 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

    Google Scholar 

  26. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  27. 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  28. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  30. 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

    PubMed  PubMed Central  Article  Google Scholar 

  31. 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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    PubMed  PubMed Central  Article  Google Scholar 

  34. 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

    CAS  PubMed  Article  Google Scholar 

  35. 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

    PubMed  Article  CAS  Google Scholar 

  36. 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

    CAS  PubMed  Article  Google Scholar 

  37. 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 

  38. 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

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

    Google Scholar 

  40. 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 

  41. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  42. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  44. 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 

  45. 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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  49. 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

    Google Scholar 

  50. 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

    CAS  PubMed  Article  Google Scholar 

  51. 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

    PubMed  Article  Google Scholar 

  52. 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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  54. 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

    CAS  PubMed  Article  Google Scholar 

  55. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  58. 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

    CAS  PubMed  Article  Google Scholar 

  59. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  60. 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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  62. 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

    CAS  PubMed  Article  Google Scholar 

  63. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  64. 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

    CAS  PubMed  Article  Google Scholar 

  65. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  66. 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

    CAS  Article  Google Scholar 

  67. 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

    CAS  PubMed  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

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

    Google Scholar 

  70. 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

    CAS  Article  PubMed  Google Scholar 

  71. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  73. 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

    CAS  PubMed  Article  Google Scholar 

  74. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  78. 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

    Google Scholar 

  79. 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

  80. 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 

  81. 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

    CAS  PubMed  Article  Google Scholar 

  82. 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  83. 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

    CAS  PubMed  Article  Google Scholar 

  84. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  85. 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 

  86. 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  87. 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

    PubMed Central  Article  CAS  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  89. 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

    Google Scholar 

  90. 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

    Google Scholar 

  91. 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 

  92. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  93. 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

    CAS  PubMed  Article  Google Scholar 

  94. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  95. 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

    CAS  PubMed  Article  Google Scholar 

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

    Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  98. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  99. 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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  101. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  102. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  103. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  104. 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

    CAS  PubMed  Article  Google Scholar 

  105. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  106. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  107. 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 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  109. 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

    PubMed  Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  111. 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

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

    CAS  PubMed  Article  Google Scholar 

  113. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  114. 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

    CAS  PubMed  Article  Google Scholar 

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

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

    CAS  PubMed  Article  Google Scholar 

  117. 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

    PubMed  Article  CAS  Google Scholar 

  118. 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 

  119. 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

    CAS  Article  Google Scholar 

  120. 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

  121. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  122. 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

    CAS  PubMed  Article  Google Scholar 

  123. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  124. 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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

  127. 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 

  128. 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 

  129. 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

    CAS  PubMed  Article  Google Scholar 

  130. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  131. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  132. 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

    CAS  PubMed  Article  Google Scholar 

  133. 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

    CAS  PubMed  Article  Google Scholar 

  134. 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

    CAS  PubMed  Article  Google Scholar 

  135. 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

    Google Scholar 

  136. 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 

  137. 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

  138. 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 

  139. 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

    CAS  PubMed  Article  Google Scholar 

  140. 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

    CAS  PubMed  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  144. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  145. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  146. 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

    CAS  PubMed  Article  Google Scholar 

  147. 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

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

    PubMed  Article  Google Scholar 

  149. 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

    PubMed  Article  CAS  Google Scholar 

  150. 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

    CAS  PubMed  Article  Google Scholar 

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

    Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  154. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  155. 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

    CAS  PubMed  Article  Google Scholar 

  156. 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

    CAS  PubMed  Article  Google Scholar 

  157. 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

    CAS  PubMed  Article  Google Scholar 

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

    PubMed  PubMed Central  Article  Google Scholar 

  159. 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

    CAS  PubMed  Article  Google Scholar 

  160. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  161. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  162. 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

    CAS  PubMed  Article  Google Scholar 

  163. 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

    PubMed  PubMed Central  Article  CAS  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  165. 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 

  166. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  167. 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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to B M Ribeiro.

Additional information

Publisher’s Note

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

Edited by Lessando Moreira Gontijo – UFV

Rights and permissions

Reprints and Permissions

About this article

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

Keywords

  • Insect viruses
  • baculoviruses
  • biological control
  • RNA insect viruses
  • DNA insect viruses