Abstract
Granuloviruses (GVs) Betabaculovirus associated with the fall armyworm (FAW), Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae), especially those of the type I, have scarcely been studied. These GVs might be an effective alternative for the biocontrol of this insect. In this study, the native GVs SfGV-CH13 and SfGV-CH28 were isolated from FAW larvae and characterized for morphology, molecular traits, and insecticidal activity. The elapsed time between symptomatic infection of larvae and stop feeding as well as the weight of larvae before death or prior to pupation were also evaluated. Both GVs had ovoid shape and a length of 0.4 µm. They had the same DNA restriction profiles and their genome sizes were about 126 kb. The symptomatic infection with the tested GVs mainly caused flaccidity of larva body and discoloration of integument. The integument lysis was only observed in 8% of infected larvae. Infected larvae gradually stopped feeding. Overall, these symptoms are characteristic of infections caused by type I GVs, which are known as monoorganotropic or slow-killing GVs. The median lethal dose (LD50) values for SfGV-CH13 and SfGV-CH28 isolates were 5.4 × 102 and 1.1 × 103 OBs/larva, respectively. The median lethal time (LT50) ranged from 17 to 24 days. LT50 values decreased as the viral dose was increased. The elapsed time from symptomatic infection until pupation and body weight of larvae (third instar) were higher with SfGV-CH28 than SfGV-CH13. Both granulovirus isolates were able to kill the FAW larvae from the 12th day.
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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
Code Availability
Not applicable.
References
Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267. https://doi.org/10.1093/jee/18.2.265a
Ali G, Abma-Henkens MH, van der Werf W, Hemerik L, Vlak JM (2018) Genotype assembly, biological activity and adaptation of spatially separated isolates of Spodoptera litura nucleopolyhedrovirus. J Invertbr Pathol 153:20–29. https://doi.org/10.1016/j.jip.2018.01.009
Alletti GG, Eigenbrod M, Carstens EB, Kleespies RG, Jehle JA (2017) The genome sequence of Agrotis segetum granulovirus, isolate AgseGV-DA, reveals a new Betabaculovirus species of a slow killing granulovirus. J Invertbr Pathol 146:58–68. https://doi.org/10.1016/j.jip.2017.04.008
Barrera G, Simón O, Villamizar L, Williams T, Caballero P (2011) Spodoptera frugiperda multiple nucleopolyhedrovirus as a potential biological insecticide: genetic and phenotypic comparison of field isolates from Colombia. Biol Control 58:113–120. https://doi.org/10.1016/j.biocontrol.2011.04.009
Barrera G, Gómez J, Cuartas P, León G, Villamizar L (2014) Characterization of a Colombian isolate of Erinnyis ello granulovirus (L)(Lepidoptera: Sphingidae). Rev Colomb Biotecnol 16:129–140. https://doi.org/10.15446/rev.colomb.biote.v16n2.41663
Bhandari K, Sood P, Mehta PK, Choudhary A (2010) Effect of granulosis virus infection on food consumption and utilization by Pieris brassicae (Linnaeus). JBC 24:65–69
Biedma ME, Salvador R, Ferrelli ML, Sciocco-Cap A, Romanowski V (2015) Effect of the interaction between Anticarsia gemmatalis multiple nucleopolyhedrovirus and Epinotia aporema granulovirus, on A. gemmatalis (Lepidoptera: Noctuidae) larvae. Biol Control 91:17–21. https://doi.org/10.1016/j.biocontrol.2015.07.006
Bivian-Hernández MdlÁ, López-Tlacomulco J, Mares-Mares E, Ibarra JE, Del Rincón-Castro MC (2017) Genomic analysis of a Trichoplusia ni Betabaculovirus (TnGV) with three different viral enhancing factors and two unique genes. Arch Virol 162:3705–3715. https://doi.org/10.1007/s00705-017-3506-y
Blanco CA, Pellegaud JG, Nava-Camberos U, Lugo-Barrera D, Vega-Aquino P, Coello J, Terán-Vargas AP, Vargas-Camplis J (2014) Maize pests in Mexico and challenges for the adoption of integrated pest management programs. J Integr Pest Manag 5:E1–E9. https://doi.org/10.1603/IPM14006
Bustillos-Rodríguez JC, Ordóñez-García M, Ornelas-Paz JdJ, Sepúlveda-Ahumada DR, Zamudio-Flores PB, Acosta-Muñiz CH, Gallegos-Morales G, Berlanga-Reyes DI, Rios-Velasco C (2023) Effect of high temperature and UV radiation on the insecticidal capacity of a Spodoptera frugiperda nucleopolyhedrovirus microencapsulated in a matrix based on oxidized corn starch. Neotrop Entomol 52:104–113. https://doi.org/10.1007/s13744-022-01016-y
Caballero P, Williams T, López-Ferber M (2001) Estructura y clasificación de los baculovirus. In: Caballero P, Williams T, López-Ferber M (eds) Los baculovirus y sus aplicaciones como bioinsecticidas en el control biológico de plagas. Universidad Pública de Navarra-Phytoma, Valencia, Spain, pp 15–46
Casmuz A, Juárez ML, Socías MG, Murúa MG, Prieto S, Medina S, Willink E, Gastaminza G (2010) Revisión de los hospederos del gusano cogollero del maíz, Spodoptera frugiperda (Lepidoptera: Noctuidae). Rev Soc Entomol Arge 69:209–23 (https://www.redalyc.org/articulo.oa?id=322028487010)
Cuartas P, Barrera G, Barreto E, Villamizar L (2014) Characterisation of a colombian granulovirus (Baculoviridae: Betabaculovirus) isolated from Spodoptera frugiperda (lepidoptera: Noctuidae) larvae. Biocontrol Sci Techn 24:1265–1285. https://doi.org/10.1080/09583157.2014.933312
Cuartas PE, Barrera GP, Belaich MN, Barreto E, Ghiringhelli PD, Villamizar LF (2015) The complete sequence of the first Spodoptera frugiperda Betabaculovirus genome: a natural multiple recombinant virus. Viruses 7:394–421. https://doi.org/10.3390/v7010394
Cuartas-Otálora PE, Gómez-Valderrama JA, Ramos AE, Barrera-Cubillos GP, Villamizar-Rivero LF (2019) Bio-insecticidal potential of nucleopolyhedrovirus and granulovirus mixtures to control the fall armyworm Spodoptera frugiperda (JE Smith, 1797)(Lepidoptera: Noctuidae). Viruses 11:684. https://doi.org/10.3390/v11080684
Espinel-Correal C, López-Ferber M, Zeddam JL, Villamizar L, Gómez J, Cotes AM, Léry X (2012) Experimental mixtures of Phthorimaea operculella granulovirus isolates provide high biological efficacy on both Phthorimaea operculella and Tecia solanivora (Lepidoptera: Gelechiidae). J Invertbr Pathol 110:375–381. https://doi.org/10.1016/j.jip.2012.04.012
Federici BA (1997) Baculovirus pathogenesis. In: Miller LK (ed) The baculoviruses. Springer, US, Boston, MA, pp 33–59
Ferrelli ML, Pidre ML, Ghiringhelli PD, Torres S, Fabre ML, Masson T, Cédola MT, Sciocco-Cap A, Romanowski V (2018) Genomic analysis of an Argentinean isolate of Spodoptera frugiperda granulovirus reveals that various baculoviruses code for Lef-7 proteins with three F-box domains. PLoS ONE 13:e0202598. https://doi.org/10.1371/journal.pone.0202598
Finney DJ (1971) Probit analysis. Cambridge University Press, New York
García-Banderas D, Tamayo-Mejía F, Pineda S, de la Rosa JIF, Lasa R, Chavarrieta-Yáñez JM, Gervasio-Rosas E, Zamora-Avilés N, Morales SI, Ramos-Ortiz S (2020) Biological characterization of two Spodoptera frugiperda nucleopolyhedrovirus isolates from Mexico and evaluation of one isolate in a small-scale field trial. Biol Control 149:104316. https://doi.org/10.1016/j.biocontrol.2020.104316
Gómez JA, Guevara EJ, Barrera GP, Cotes AM, Villamizar LF (2010) Aislamiento, identificación y caracterización de nucleopoliedrovirus nativos de Spodoptera frugiperda en Colombia. Rev Fac Nac Agron Medellin 63:5511–5520 (https://www.redalyc.org/articulo.oa?id=1799/179918602005)
Gutiérrez-Moreno R, Mota-Sanchez D, Blanco CA, Whalon ME, Terán-Santofimio H, Rodriguez-Maciel JC, DiFonzo C (2019) Field-evolved resistance of the fall armyworm (Lepidoptera: Noctuidae) to synthetic insecticides in Puerto Rico and Mexico. J Econ Entomol 112:792–802. https://doi.org/10.1093/jee/toy372
Haase S, Sciocco-Cap A, Romanowski V (2015) Baculovirus insecticides in Latin America: historical overview, current status and future perspectives. Viruses 7:2230–2267. https://doi.org/10.3390/v7052230
Hackett KJ, Boore A, Deming C, Buckley E, Camp M, Shapiro M (2000) Helicoverpa armigera granulovirus interference with progression of H. zea nucleopolyhedrovirus disease in H. zea larvae. J Invertbr Pathol 75:99–106. https://doi.org/10.1006/jipa.1999.4914
Hafez AM, Mota-Sanchez D, Vandervoort C, Wise JC (2021) Resistance affects the field performance of insecticides used for control of Choristoneura rosaceana in Michigan apples and cherries. Insects 12:846. https://doi.org/10.3390/insects12090846
Hatem AE-S, Aldebis HK, Osuna EV (2011) Effects of the Spodoptera littoralis granulovirus on the development and reproduction of cotton leafworm S. littoralis. Biol Control 59:192–199. https://doi.org/10.1016/j.biocontrol.2011.07.004
Herniou E, Arif B, Becnel J, Blissard G, Bonning B, Harrison R, Jehle J, Theilmann D, Vlak J (2011) Baculoviridae. In: King A, Adams M, Carstens E, Lefkowits E (eds) Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. Academic Press, Amsterdam, pp 163–173
Hilton S, Winstanley D (2008) Biological characterization of an English granulovirus from the summer fruit tortrix moth, Adoxophyes orana. J Invertbr Pathol 97:298–305. https://doi.org/10.1016/j.jip.2007.09.011
Hinsberger A, Theulier Saint Germain S, Guerrero P, Blachère-López C, López-Ferber M, Bayle S (2019) A combination of real-time PCR and high-resolution melting analysis to detect and identify CpGV genotypes involved in type I resistance. Viruses 11:723. https://doi.org/10.3390/v11080723
Hughes P, Wood H (1981) A synchronous peroral technique for the bioassay of insect viruses. J Invertebr Pathol 37:154–159. https://doi.org/10.1016/0022-2011(81)90069-0
Hussain AG, Wennmann JT, Goergen G, Bryon A, Ros VI (2021) Viruses of the fall armyworm Spodoptera frugiperda: a review with prospects for biological control. Viruses 13:2220. https://doi.org/10.3390/v13112220
Ikeda M, Hamajima R, Kobayashi M (2015) Baculoviruses: diversity, evolution and manipulation of insects. Entomol Sci 18:1–20. https://doi.org/10.1111/ens.12105
Inceoglu AB, Kamita SG, Hammock BD (2006) Genetically modified baculoviruses: a historical overview and future outlook. Adv Virus Res 68:323–360. https://doi.org/10.1016/S0065-3527(06)68009-3
Inceoglu AB, Kamita SG, Hinton AC, Huang Q, Severson, T F K, K D, Hammock BD (2001) Recombinant baculoviruses for insect control. Pest Manag Sci 57:981-987https://doi.org/10.1002/ps.393
Ishimwe E, Hodgson JJ, Passarelli AL (2015) Expression of the Cydia pomonella granulovirus matrix metalloprotease enhances Autographa californica multiple nucleopolyhedrovirus virulence and can partially substitute for viral cathepsin. Virology 481:166–178. https://doi.org/10.1016/j.virol.2015.02.022
Jehle JA, Blissard G, Bonning B, Cory J, Herniou E, Rohrmann G, Theilmann D, Thiem S, Vlak J (2006) On the classification and nomenclature of baculoviruses: a proposal for revision. Arch Virol 151:1257–1266. https://doi.org/10.1007/s00705-006-0763-6
Jehle J, Schulze-Bopp S, Undorf-Spahn K, Fritsch E (2017) Evidence for a second type of resistance against Cydia pomonella granulovirus in field populations of codling moths. Appl Environ Microbiol 83:e02330-e2416. https://doi.org/10.1128/AEM.02330-16
Ju D, Mota-Sanchez D, Fuentes-Contreras E, Zhang Y-L, Wang X-Q, Yang X-Q (2021) Insecticide resistance in the Cydia pomonella (L): Global status, mechanisms, and research directions. Pestic Biochem Physiol 178:104925. https://doi.org/10.1016/j.pestbp.2021.104925
Kenis M, Benelli G, Biondi A et al (2022) Invasiveness, biology, ecology, and management of the fall armyworm, Spodoptera frugiperda. Entomol Gen 2:187–241. https://doi.org/10.1127/entomologia/2022/1659
Kumar PN, Prasad YG, Prabhakar M, Shanker AK, Bhanu D (2017) Molecular and in silico characterization of Achaea janata granulovirus granulin gene. Interdiscip Sci 9:528–539. https://doi.org/10.1007/s12539-016-0159-6
Luque T, Finch R, Crook N, O’Reilly DR, Winstanley D (2001) The complete sequence of the Cydia pomonella granulovirus genome. J Gen Virol 82:2531–2547. https://doi.org/10.1099/0022-1317-82-10-2531
Machado EP, dos S Rodrigues Junior GL, Somavilla JC, Führ FM, Zago SL, Marques LH, Santos AC, Nowatzki T, Dahmer ML, Omoto C (2020) Survival and development of Spodoptera eridania, Spodoptera cosmioides and Spodoptera albula (Lepidoptera: Noctuidae) on genetically-modified soybean expressing Cry1Ac and Cry1F proteins. Pest Manag Sci 76:4029–4035. https://doi.org/10.1002/ps.5955
Moscardi F (1999) Assessment of the application of baculoviruses for control of Lepidoptera. Annu Rev Entomol 44:257–289. https://doi.org/10.1146/annurev.ento.44.1.257
Muñoz D, Martínez AM, Pérez RM, de Escudero Fuentemilla IR, Vilaplana L (2001) Técnicas básicas para la caracterización de baculovirus. In: Caballero P, Williams T, López-Ferber M (eds) Los baculovirus y sus aplicaciones como bioinsecticidas en el control biológico de plagas. Universidad Pública de Navarra-Phytoma, Valencia, Spain, pp 479–518
Ordóñez-García M, Rios-Velasco C, Berlanga-Reyes DI, Acosta-Muñiz CH, Salas-Marina MÁ, Cambero-Campos OJ (2015) Occurrence of natural enemies of Spodoptera frugiperda (Lepidoptera: Noctuidae) in Chihuahua, Mexico. Fla Entomol 98:843–847 (https://www.jstor.org/stable/24587732)
Ordóñez-García M, Rios-Velasco C, Ornelas-Paz JdJ, Bustillos-Rodríguez JC, Acosta-Muñiz CH, Berlanga-Reyes DI, Salas-Marina MÁ, Cambero-Campos OJ, Gallegos-Morales G (2020) Molecular and morphological characterization of multiple nucleopolyhedrovirus from Mexico and their insecticidal activity against Spodoptera frugiperda (Lepidoptera: Noctuidae). J Appl Entomol 144:123–132. https://doi.org/10.1111/jen.12715
Pauli G, Moura Mascarin G, Eilenberg J, Delalibera Júnior I (2018) Within-host competition between two entomopathogenic fungi and a granulovirus in Diatraea saccharalis (Lepidoptera: Crambidae). Insects 9:64. https://doi.org/10.3390/insects9020064
Pidre ML, Sabalette KB, Romanowski V, Ferrelli ML (2019) Identification of an Argentinean isolate of Spodoptera frugiperda granulovirus. Rev Argent Microbiol 51:381–385. https://doi.org/10.1016/j.ram.2018.10.003
Rohrmann GF (2019) The baculovirus replication cycle: effects on cells and insects. Baculovirus Molecular Biology. 4th edition. National Center for Biotechnology Information (US), Oregon, USA, pp 57–82
Sagar G, Aastha B, Laxman K (2020) An introduction of fall armyworm (Spodoptera frugiperda) with management strategies: a review paper. Nippon J Environ Sci 1:1010. https://doi.org/10.46266/njes.1010
SAS I (2002) SAS user guide, version 9.0. SAS Institute Incorporated, Cary NC, USA
Sauer AJ, Fritsch E, Undorf-Spahn K, Nguyen P, Marec F, Heckel DG, Jehle JA (2017) Novel resistance to Cydia pomonella granulovirus (CpGV) in codling moth shows autosomal and dominant inheritance and confers cross-resistance to different CpGV genome groups. PLoS ONE 12:e0179157. https://doi.org/10.1371/journal.pone.017915
Sciocco-Cap A (2001) Biología y patogénesis de los baculovirus. In: Caballero P, Williams T, López-Ferber M (eds) Los baculovirus y sus aplicaciones como bioinsecticidas en el control biológico de plagas. Universidad Pública de Navarra-Phytoma, Valencia, Spain, pp 47–72
Shapiro M (2000) Effect of two granulosis viruses on the activity of the gypsy moth (Lepidoptera: Lymantriidae) nuclear polyhedrosis virus. J Econ Entomol 93:1633–1637. https://doi.org/10.1603/0022-0493-93.6.1633
Sporleder M, Rodriguez Cauti EM, Huber J and Kroschel J (2007) Susceptibility of Phthorimaea operculella Zeller (Lepidoptera; Gelechiidae) to its granulovirus PoGV with larval age. 9: 271–278. https://doi.org/10.1111/j.1461-9563.2007.00341.x
Takahashi M, Nakai M, Saito Y, Sato Y, Ishijima C, Kunimi Y (2015) Field efficacy and transmission of fast-and slow-killing nucleopolyhedroviruses that are infectious to Adoxophyes honmai (Lepidoptera: Tortricidae). Viruses 7:1271–1283. https://doi.org/10.3390/v7031271
Wang Y, Choi JY, Roh JY, Woo SD, ** BR, Je YH (2008) Molecular and phylogenetic characterization of Spodoptera litura granulovirus. J Microbiol 46:704–708. https://doi.org/10.1007/s12275-008-0133-z
Williams T, Melo-Molina GdC, Jiménez-Fernández JA, Weissenberger H, Gómez-Díaz JS, Navarro-de-la-Fuente L, Richards AR (2023) Presence of Spodoptera frugiperda multiple Nucleopolyhedrovirus (SfMNPV) occlusion bodies in maize field soils of mesoamerica. Insects 14:80. https://doi.org/10.3390/insects14010080
Zhang D-d, **ao Y-t, Xu P-j, Yang X-m, Q-l Wu, Wu K-m (2021) Insecticide resistance monitoring for the invasive populations of fall armyworm, Spodoptera frugiperda in China. J Integr Agric 20:783–791. https://doi.org/10.1016/S2095-3119(20)63392-5
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Magali Ordóñez García thanks the Consejo Nacional de Ciencia y Tecnología (CONACYT–México) for the provided PhD scholarship.
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This research was supported by the Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación (SAGARPA-COFUPRO, México; No. CH1600001442).
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All authors contributed to the study conception and design. MOG designed research, conducted experiments, and wrote the manuscript. JCBR conducted experiments. JJOP wrote and edited the manuscript. CHAM and MASM analyzed data and edited the manuscript. OJCC and MOEV interpreted data and edited the manuscript. MAMO interpreted data and conducted research. CRV conceived research and wrote and edited the manuscript. All authors read and approved the manuscript.
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Ordóñez-García, M., Bustillos-Rodríguez, J.C., de Jesús Ornelas-Paz, J. et al. Morphological, Biological, and Molecular Characterization of Type I Granuloviruses of Spodoptera frugiperda. Neotrop Entomol (2024). https://doi.org/10.1007/s13744-024-01172-3
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DOI: https://doi.org/10.1007/s13744-024-01172-3