RNA Virus Discovery Sheds Light on the Virome of a Major Vineyard Pest, the European Grapevine Moth (Lobesia botrana)

Humberto Debat; Sebastián Gomez-Talquenca; Nicolás Bejerman

doi:10.3390/v17010095

journal article Open Access Jan 13, 2025

RNA Virus Discovery Sheds Light on the Virome of a Major Vineyard Pest, the European Grapevine Moth (Lobesia botrana)

Humberto Debat

Sebastián Gomez-Talquenca

Nicolás Bejerman

Viruses Vol. 17 No. 1 pp. 95 · MDPI AG

View at Publisher Save 10.3390/v17010095

Abstract

The European grapevine moth (Lobesia botrana) poses a significant threat to vineyards worldwide, causing extensive economic losses. While its ecological interactions and control strategies have been well studied, its associated viral diversity remains unexplored. Here, we employ high-throughput sequencing data mining to comprehensively characterize the L. botrana virome, revealing novel and diverse RNA viruses. We characterized four new viral members belonging to distinct families, with evolutionary cues of cypoviruses (Reoviridae), sobemo-like viruses (Solemoviridae), phasmaviruses (Phasmaviridae), and carmotetraviruses (Carmotetraviridae). Phylogenetic analysis of the cypoviruses places them within the genus in affinity with other moth viruses. The bi-segmented and highly divergent sobemo-like virus showed a distinctive evolutionary trajectory of its encoding proteins at the periphery of recently reported invertebrate Sobelivirales. Notably, the presence of a novel phasmavirus, typically associated with mosquitoes, expands the known host range and diversity of this family to moths. Furthermore, the identification of a carmotetravirus branching in the same cluster as the Providence virus, a lepidopteran virus which replicates in plants, raises questions regarding the biological significance of this moth virus to the grapevine host. We further explored viral sequences in several publicly available transcriptomic datasets of the moth, indicating potential prevalence across distinct conditions. These results underscore the existence of a complex virome within L. botrana and lay the foundation for future studies investigating the ecological roles, evolutionary dynamics, and potential biocontrol applications of these viruses in the L. botrana–vineyard ecosystem.

Topics

No keywords indexed for this article. Browse by subject →

References

50

[1]

Benelli "European grapevine moth, Lobesia botrana: Part I, biology and ecology" Entomol. Gen. (2023) 10.1127/entomologia/2023/1837

[2]

Fishel "Economic impact of Lobesia botrana on viticulture in Greece" J. Pest. Sci. (2020)

[3]

Ioriatti "A review of history and geographical distribution of grapevine moths in Italian vineyards in light of climate change: Looking backward to face the future" Crop. Prot. (2023) 10.1016/j.cropro.2023.106375

[4]

Simmons, G.S., Sepulveda, M.C.S., Barrios, E.A.F., Villegas, M.I., Jimenez, R.E.M., Jerez, A.R.G., Henderson, R., and Riffo, H.D. (2021). Development of sterile insect technique for control of the European grapevine moth, Lobesia botrana, in Urban areas of Chile. Insects, 12. 10.3390/insects12050378

[5]

Benelli "European grapevine moth, Lobesia botrana: Part II, prevention and management" Entomol. Gen. (2023) 10.1127/entomologia/2023/1947

[6]

Altimira, F., De La Barra, N., Godoy, P., Roa, J., Godoy, S., Vitta, N., and Tapia, E. (2022). Lobesia botrana: A biological control approach with a biopesticide based on entomopathogenic fungi in the winter season in Chile. Insects, 13. 10.3390/insects13010008

[7]

Marcucci "Occurrence of Goniozus legneri (Hymenoptera: Bethylidae) and its association to lepidopteran pests in Northern cultivated oasis of Mendoza province, Argentina" Rev. De La Soc. Entomológica Argent (2023)

[8]

Kenney "The role of environmental, virological and vector interactions in dictating biological transmission of arthropod-borne viruses by mosquitoes" Advances in Virus Research (2014) 10.1016/b978-0-12-800172-1.00002-1

[9]

Tritrophic Interactions: Microbe-Mediated Plant Effects on Insect Herbivores

Ikkei Shikano, Cristina Rosa, Ching-Wen Tan et al.

Annual Review of Phytopathology 2017 10.1146/annurev-phyto-080516-035319

[10]

Manley "Emerging viral disease risk to pollinating insects: Ecological, evolutionary and anthropogenic factors" J. Appl. Ecol. (2015) 10.1111/1365-2664.12385

[11]

Insect–plant–pathogen interactions as shaped by future climate: effects on biology, distribution, and implications for agriculture

Piotr Trębicki, Beatriz Dáder, Simone Vassiliadis et al.

Insect Science 2017 10.1111/1744-7917.12531

[12]

Debat, H.J. (2017). An RNA virome associated to the golden orb-weaver spider Nephila clavipes. Front. Microbiol., 8. 10.3389/fmicb.2017.02097

[13]

Debat "A Divergent strain of Culex pipiens-associated Tunisia virus in the malaria vector Anopheles epiroticus" Microbiol. Resour. Announc. (2018) 10.1128/mra.01026-18

[14]

Albaz "Analysis of insecticide resistance and de novo transcriptome assembly of resistance associated genes in the European grapevine moth, Lobesia botrana (Lepidoptera: Tortricidae)" Bull. Entomol. Res. (2024) 10.1017/s0007485323000640

[15]

Ding "Biosynthesis of the sex pheromone component (E, Z)-7,9-dodecadienyl acetate in the european grapevine moth, Lobesia botrana, involving ∆11 desaturation and an elusive ∆7 desaturase" J. Chem. Ecol. (2021) 10.1007/s10886-021-01252-3

[16]

Debat "Two novel flavi-like viruses shed light on the plant-infecting koshoviruses" Arch. Virol. (2023) 10.1007/s00705-023-05813-7

[17]

Debat, H., Garcia, M.L., and Bejerman, N. (2023). Expanding the repertoire of the plant-infecting Ophioviruses through metatranscriptomics data. Viruses, 15. 10.1101/2023.01.27.525910

[18]

Scarpassa, V.M., Debat, H.J., Alencar, R.B., Saraiva, J.F., Calvo, E., Arcà, B., and Ribeiro, J.M.C. (2019). An Insight into the Sialotranscriptome and Virome of Amazonian Anophelines. BMC Genom., 20. 10.1186/s12864-019-5545-0

[19]

Zhan "Isolation and genomic characterization of a cypovirus from the Oleander hawk moth, Daphnis nerii" J. Invertebr. Pathol. (2019) 10.1016/j.jip.2019.03.002

[20]

Karlin "WIV, a protein domain found in a wide number of arthropod viruses, which probably facilitates infection" J. Gen. Virol. (2024) 10.1099/jgv.0.001948

[21]

The molecular organization of cypovirus polyhedra

Fasséli Coulibaly, Elaine Chiu, Keiko Ikeda et al.

Nature 2007 10.1038/nature05628

[22]

Thézé, J., Lopez-Vaamonde, C., Cory, J.S., and Herniou, E.A. (2018). Biodiversity, evolution and ecological specialization of baculoviruses: A treasure trove for future applied research. Viruses, 10. 10.20944/preprints201806.0050.v1

[23]

Metagenomics reshapes the concepts of RNA virus evolution by revealing extensive horizontal virus transfer

Valerian V. Dolja, Eugene V. Koonin

Virus Research 2018 10.1016/j.virusres.2017.10.020

[24]

Zhao "Pathogens are an important driving force for the rapid spread of symbionts in an insect host" Nat. Ecol. Evol. (2023) 10.1038/s41559-023-02160-3

[25]

Chen, Y.P., Becnel, J.J., and Valles, S.M. (2012). RNA Viruses Infecting Pest Insects. Insect Pathology, Elsevier. 10.1016/b978-0-12-384984-7.00005-1

[26]

Kuhn "ICTV Virus Taxonomy Profile: Phasmaviridae 2024" J. Gen. Virol. (2024)

[27]

Malet, H., Williams, H.M., Cusack, S., and Rosenthal, M. (2023). The mechanism of genome replication and transcription in bunyaviruses. PLoS Pathog., 19. 10.1371/journal.ppat.1011060

[28]

Marklewitz "First isolation of an Entomobirnavirus from free-living insects" J. Gen. Virol. (2012) 10.1099/vir.0.045435-0

[29]

Dou, X., Liu, S., Soroker, V., Harari, A., and Jurenka, R. (2021). Novel RNA viruses from the transcriptome of pheromone glands in the Pink Bollworm Moth, Pectinophora gossypiella. Insects, 12. 10.3390/insects12060556

[30]

Barr "Segment specific terminal sequences of Bunyamwera bunyavirus regulate genome replication" Virology (2003) 10.1016/s0042-6822(03)00130-2

[31]

Ballinger "Discovery and evolution of bunyavirids in arctic phantom midges and ancient bunyavirid-like sequences in insect genomes" J. Virol. (2014) 10.1128/jvi.00531-14

[32]

Walter "Genome organization and translation products of Providence virus: Insight into a unique tetravirus" J. Gen. Virol. (2010) 10.1099/vir.0.023796-0

[33]

Short "Providence virus (family: Carmotetraviridae) replicates vRNA in association with the Golgi apparatus and secretory vesicles" J. Gen. Virol. (2013) 10.1099/vir.0.047647-0

[34]

Ritah "Computational characterization of providence virus non-structural proteins: Evolutionary and functional implications" J. Bioinform. Seq. Anal. (2019) 10.5897/jbsa2019.0111

[35]

Jiwaji, M., Matcher, G.F., de Bruyn, M.-M., Awando, J.A., Moodley, H., Waterworth, D., Jarvie, R.A., and Dorrington, R.A. (2019). Providence virus: An animal virus that replicates in plants or a plant virus that infects and replicates in animal cells?. PLoS ONE, 14. 10.1371/journal.pone.0217494

[36]

Matthijnssens "ICTV Virus Taxonomy Profile: Spinareoviridae 2022" J. Gen. Virol. (2022) 10.1099/jgv.0.001781

[37]

Atomic model of a cypovirus built from cryo-EM structure provides insight into the mechanism of mRNA capping

Lingpeng Cheng, Jingchen Sun, Kai Zhang et al.

Proceedings of the National Academy of Sciences 2011 10.1073/pnas.1014995108

[38]

Li "Structure of RdRps within a transcribing dsRNA virus provides insights into the mechanisms of RNA synthesis" J. Mol. Biol. (2020) 10.1016/j.jmb.2019.09.015

[39]

Liu "Cryo-EM shows the polymerase structures and a nonspooled genome within a dsRNA virus" Science (2015) 10.1126/science.aaa4938

[40]

3.88 Å structure of cytoplasmic polyhedrosis virus by cryo-electron microscopy

Xuekui Yu, Lei Jin, Z. Hong Zhou

Nature 2008 10.1038/nature06893

[41]

Zhang "In situ structures of the segmented genome and RNA polymerase complex inside a dsRNA virus" Nature (2015) 10.1038/nature15767

[42]

Zhan "Isolation and genomic characterization of a cypovirus from Clanis bilineata" Virus Genes (2023) 10.1007/s11262-023-02029-4

[43]

Martemyanov, V.V., Akhanaev, Y.B., Belousova, I.A., Pavlusin, S.V., Yakimova, M.E., Kharlamova, D.D., Ageev, A.A., Golovina, A.N., Astapenko, S.A., and Kolosov, A.V. (2023). A new cypovirus-1 strain as a promising agent for Lepidopteran pest control. Microbiol. Spectr., 11. 10.1128/spectrum.03855-22

[44]

Kuang "Transcriptional responses of Daphnis nerii larval midgut to oral infection by Daphnis nerii cypovirus-23" Virol. J. (2021) 10.1186/s12985-021-01721-x

[45]

Fargette "ICTV Virus Taxonomy Profile: Solemoviridae 2021" J. Gen. Virol. (2021)

[46]

Divergent RNA viruses infecting sea lice, major ectoparasites of fish

Tianyi Chang, Brian P. V. Hunt, Junya Hirai et al.

PLOS Pathogens 10.1371/journal.ppat.1011386

[47]

Redefining the invertebrate RNA virosphere

Mang Shi, Xian-Dan Lin, Jun-Hua Tian et al.

Nature 2016 10.1038/nature20167

[48]

Shotgun Metagenomic Sequencing Reveals Virome Composition of Mosquitoes from a Transition Ecosystem of North-Northeast Brazil

Carine Fortes Aragão, Sandro Patroca da Silva, Bruna Laís Sena do Nascimento et al.

Genes 10.3390/genes14071443

[49]

Dissecting the Species-Specific Virome in Culicoides of Thrace

Konstantinos Konstantinidis, Maria Bampali, Michael de Courcy Williams et al.

Frontiers in Microbiology 10.3389/fmicb.2022.802577

[50]

Ottati, S., Chiapello, M., Galetto, L., Bosco, D., Marzachì, C., and Abbà, S. (2020). New viral sequences identified in the Flavescence Dorée phytoplasma vector Scaphoideus titanus. Viruses, 12. 10.3390/v12030287

Metrics

2

Citations

50

References

Details

Published: Jan 13, 2025
Vol/Issue: 17(1)
Pages: 95
License: View

Authors

H

Humberto Debat

Instituto de Patología Vegetal, Centro de Investigaciones Agropecuarias, Instituto Nacional de Tecnología Agropecuaria (IPAVE-CIAP-INTA), Camino 60 Cuadras Km 5,5, Córdoba X5020ICA, Argentina; Unidad de Fitopatología y Modelización Agrícola, Consejo Nacional de Investigaciones Científicas y Técnicas (UFYMA-CONICET), Camino 60 Cuadras Km 5,5, Córdoba X5020ICA, Argentina

S

Sebastián Gomez-Talquenca

Estación Experimental Agropecuaria Mendoza, Instituto Nacional de Tecnología Agropecuaria (EEA-Mendoza-INTA), San Martín 3853, Luján de Cuyo, Mendoza 5507, Argentina

N

Nicolás Bejerman

Instituto de Patología Vegetal, Centro de Investigaciones Agropecuarias, Instituto Nacional de Tecnología Agropecuaria (IPAVE-CIAP-INTA), Camino 60 Cuadras Km 5,5, Córdoba X5020ICA, Argentina; Unidad de Fitopatología y Modelización Agrícola, Consejo Nacional de Investigaciones Científicas y Técnicas (UFYMA-CONICET), Camino 60 Cuadras Km 5,5, Córdoba X5020ICA, Argentina

Cite This Article

Humberto Debat, Sebastián Gomez-Talquenca, Nicolás Bejerman (2025). RNA Virus Discovery Sheds Light on the Virome of a Major Vineyard Pest, the European Grapevine Moth (Lobesia botrana). Viruses, 17(1), 95. https://doi.org/10.3390/v17010095

RNA Virus Discovery Sheds Light on the Virome of a Major Vineyard Pest, the European Grapevine Moth (Lobesia botrana)

You May Also Like