Natural populations of Spodoptera exigua are infected by multiple viruses that are transmitted to their offspring

Journal of Invertebrate Pathology

Volumn 122, Issue , 2014, Pages 22-27

  Virto, Cristina ^a,b   Navarro, David ^c   Tellez, M Mar ^c   Herrero, Salvador ^d   Williams, Trevor ^e   Murillo, Rosa ^a,b   Caballero, Primitivo ^a,b  

^a CSIC   (Spain)

^b PUBLIC UNIVERSITY OF NAVARRE   (Spain)

^c IFAPA CENTRO EL TORUÑO   (Spain)

^d UNIVERSITY OF VALENCIA   (Spain)

^e INSTITUTO DE ECOLOGÍA   (Mexico)

Author keywords

Adult infection; Alphabaculovirus; Co infection; Iflavirus; SeMNPV

Indexed keywords

ANIMAL; BACULOVIRIDAE; BIOLOGICAL PEST CONTROL; FEMALE; MALE; PREVALENCE; PROCEDURES; RNA VIRUS; SPAIN; SPODOPTERA; VIROLOGY;

ANIMALS; FEMALE; MALE; NUCLEOPOLYHEDROVIRUS; PEST CONTROL, BIOLOGICAL; PREVALENCE; RNA VIRUSES; SPAIN; SPODOPTERA;

EID: 84907168812     PISSN: 00222011     EISSN: 10960805     Source Type: Journal    
DOI: 10.1016/j.jip.2014.07.007     Document Type: Article

References (38)

1. Bianchi F.J.J.A., van Essen P.H.A., van der Werf W., Smits P.H. Transmission dynamics of the multicapsid nucleopolyhedrovirus SeMNPV in Spodoptera exigua populations in greenhouse chrysanthemum. Proc. Exper. Appl. Entomol. 2001, 12:91-96.
2. Burand J., Kim W., Welch A., Elkinton J.S. Identification of a nucleopolyhedrovirus in winter moth populations from Massachusetts. J. Invertebr. Pathol. 2011, 108:217-219.
3. Burden J.P., Griffiths C.M., Cory J.S., Smith P., Sait S.M. Vertical transmission of sublethal granulovirus infection in the Indian meal moth, Plodia interpunctella. Mol. Ecol. 2002, 11:547-555.
4. Burden J.P., Nixon C.P., Hodgkinson A.E., Possee R.D., Sait S.M., King L.A., Hails R.S. Covert infections as a mechanism for long-term persistence of baculoviruses. Ecol. Lett. 2003, 6:524-531.
5. Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L., Vandesompele J., Wittwer C.T. The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009, 55:611-622.
6. Caballero P., Aldebis H.K., Vargas-Osuna E., Santiago-Alvarez C. Epizootics caused by a nuclear polyhedrosis virus in populations of Spodoptera exigua in southern Spain. Biocontrol Sci. Technol. 1992, 2:35-38.
7. Cabodevilla O., Ibañez I., Simo´n O., Murillo R., Caballero P., Williams T. Occlusion body pathogenicity, virulence and productivity traits vary with transmission strategy in a nucleopolyhedrovirus. Biol. Control 2011, 56:184-192.
8. Cabodevilla O., Villar E., Virto C., Murillo R., Williams T., Caballero P. Intra- and intergenerational persistence of an insect nucleopolyhedrovirus: Adverse effects of sublethal disease on host development, reproduction, and susceptibility to superinfection. Appl. Environ. Microbiol. 2011, 77:2954-2960.
9. Choi J.Y., Kim Y., Wang Y., Shin S.W., Kim I., Tao X.Y., Liu Q., Roh J.Y., Kim J.S., Je Y.H. Complete genome sequence of a novel picorna-like virus isolated from Spodoptera exigua. J. Asia-Pac. Entomol. 2012, 15:259-263.
10. Cory J.S., Myers J.H. The ecology evolution of insect baculoviruses. Ann. Rev. Ecol. Syst. 2003, 34:239-272.
11. Crawley M.J. GLIM for Ecologists 1993, Blackwell Sci., Oxford, UK.
12. Elvira S., Williams T., Caballero P. Juvenile hormone analog technology: Effects on larval cannibalism and the production of Spodoptera exigua (Lepidoptera: Noctuidae) nucleopolyhedrovirus. J. Econ. Entomol. 2010, 103:577-582.
13. Glaser R.L., Meola M.A. The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile Virus infection. PLoS ONE 2010, 5:e11977.
14. Graham R.I., Grzywacz D., Mushobozi W.L., Wilson K. Wolbachia in a major African crop pest increases susceptibility to viral disease rather than protects. Ecol. Lett. 2012, 15:993-1000.
15. Hughes D.S., Possee R.D., King L.A. Activation and detection of a latent baculovirus resembling Mamestra brassicae nuclear polyhedrosis virus in M. brassicae insects. Virology 1993, 194:608-615.
16. Jakubowska A.K., D'Angiolo M., Gonza´lez-Marti´nez R.M., Milla´n-Leiva A., Carballo A., Murillo R., Caballero P.Herrero, S. Simultaneous occurrence of covert infections with small RNA viruses in the lepidopteran Spodoptera exigua. J. Invertebr. Pathol. 2014, http://dx.doi.org/10.1016/j.jip.2014.06.009.
17. Kemp E.M., Woodward D.T., Cory J.S. Detection of single and mixed covert baculovirus infections in eastern spruce budworm, Choristoneura fumiferana populations. J. Invertebr. Pathol. 2011, 107:202-205.
18. Kolodny-Hirsch D.M., Sitchawat T., Jansari J., Chenrchaivachirakul A., Ketunuti U. Field evaluation of a commercial formulation of the Spodoptera exigua (Lepidoptera: Noctuidae) nuclear polyhedrosis virus for control of beet armyworm on vegetable crops in Thailand. Biocontr. Sci. Technol. 1997, 7:475-488.
19. Kouassi L.N., Tsuda K., Goto C., Mukawa S., Sakamaki Y., Kusigemati K., Nakamura M. Prevalence of latent virus in Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae) and its activation by a heterologous virus. Appl. Entomol. Zool. 2009, 44:95-102.
20. Krokene P., Heldal I., Fossdal C.G. Quantifying Neodipron nucleopolyhedrovirus DNA from insects, foliage and forest litter using the quantitative real-time polymerase chain reaction. Agric. Forest Entomol. 2013, 15:120-125.
21. Lasa R., Ruiz-Portero C., Alcazar M.D., Belda J.E., Caballero P., Williams T. Efficacy of Spodoptera exigua multiple nucleopolyhedrovirus as a biological insecticide for beet armyworm control in greenhouses of southern Spain. Biocontrol Sci. Technol. 2007, 17:221-232.
22. Milla´n-Leiva A., Jakubowska A.K., Ferre J., Herrero S. Genome sequence of SeIV-1, a novel virus from the Iflaviridae family infective to Spodoptera exigua. J. Invertebr. Pathol. 2012, 109:127-133.
23. Murakami R., Suetsugu Y., Kobayashi T., Nakashima N. The genome sequence and transmission of an iflavirus from the brown planthopper, Nilavarpa lugens. Virus Res. 2013, 176:179-187.
24. Murillo R., Hussey M.S., Possee R.D. Evidence for covert baculovirus infections in a Spodoptera exigua laboratory culture. J. Gen. Virol. 2011, 92:1061-1070.
25. Numerical Algorithms Group The GLIM System: Release 4 Manual 1993, Clarendon Press, Oxford, UK. B. Francis, C. Green, C. Payne (Eds.).
26. Ongus J.R., Peters D., Bonmatin J.M., Bengsch E., Vlak J.M., van Oers M.M. Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. J. Gen. Virol. 2004, 85:3747-3755.
27. Pascual L., Jakubowska A.K., Blanca J.M., Cañizares J., Ferre´ J., Gloeckner G., Vogel H., Herrero S. The transcriptome of Spodoptera exigua larvae exposed to different types of microbes. Insect Biochem. Mol. Biol. 2012, 42:557-570.
28. Smits P.H., Vlak J.M. Biological activity of Spodoptera exigua nuclear polyhedrosis virus against S. exigua larvae. J. Invertebr. Pathol. 1988, 52:107-114.
29. Smits P.H., Vlak J.M. Registration of the first viral insecticide in the Netherlands: the development of Spod-X based on Spodoptera exigua nuclear polyhedrosis virus. Meded. Fac. Landbouwwet., Rijksuniv. Gent 1994, 59:385-392.
30. The´ze´ J., Cabodevilla O., Palma L., Williams T., Caballero P., Herniou E.A. Genomic Diversity in European Spodoptera exigua multiple nucleopolyhedrovirus isolates. J. Gen. Virol. 2014, 10.1099/vir.0.064766-0.
31. Vail P.V., Morris T.J., Collier S.S., Mackey B. An RNA virus in Autographa californica nuclear polyhedrosis virus preparations: Incidence and influence on baculovirus activity. J. Invertebr. Pathol. 1983, 41:171-178.
32. Vail P.V., Morris T.J., Collier S.S. An RNA virus in Autographa californica nuclear polyhedrosis virus preparations: Gross pathology and infectivity. J. Invertebr. Pathol. 1983, 41:179-183.
33. van Oers M.M. Genomics and biology of Iflaviruses. Insect Virology 2010, 231-250. Caister Academic Press, Norfolk, UK. S. Asgari, K. Johnson (Eds.).
34. Vilaplana L., Wilson K., Redman E., Cory J. Pathogen persistence in migratory insects: High levels of vertically-transmitted virus infection in field populations of the African armyworm. Evol. Ecol. 2010, 24:147-160.
35. Virto C., Za´rate C.A., Lo´pez-Ferber M., Murillo R., Caballero P., Williams T. Gender-mediated differences in vertical transmission of Spodoptera exigua multiple nucleopolyhedrovirus (SeMNPV). PLoS ONE 2013, 8:e70932.
36. Wang C.H., Wu C.Y., Lo C.F. A new picorna-like virus, PnPV, isolated from Ficus Transparent wing moth, Perina nuda (Fabricius). J. Invertebr. Pathol. 1999, 74:62-68.
37. Wang X., Zhang J., Lu J., Yi F., Liu C., Hu Y. Sequence analysis and genomic organization of a new insect picorna-like virus, Ectropis obliqua picorna-like virus, isolated from Ectropis obliqua. J. Gen. Virol. 2004, 85:1145-1151.
38. Yue C., Schroder M., Gisder S., Genersch E. Vertical-transmission routes for deformed wing virus of honeybees (Apis mellifera). J. Gen. Virol. 2007, 88:2329-2336.