Complex interactions among insect viruses-insect vector-arboviruses

Hui Wang, Qian Chen, Taiyun Wei

PDF
Insect Science ›› 2024, Vol. 31 ›› Issue (3) : 683-693. DOI: 10.1111/1744-7917.13285
REVIEW

Complex interactions among insect viruses-insect vector-arboviruses

Author information +
History +

Abstract

Insects are the host or vector of diverse viruses including those that infect vertebrates, plants, and fungi. Insect viruses reside inside their insect hosts and are vertically transmitted from parent to offspring. The insect virus–host relationship is intricate, as these viruses can impact various aspects of insect biology, such as development, reproduction, sex ratios, and immunity. Arthropod-borne viruses (arboviruses) that cause substantial global health or agricultural problems can also be vertically transmitted to insect vector progeny. Multiple infections with insect viruses and arboviruses are common in nature. Such coinfections involve complex interactions, including synergism, dependence, and antagonism. Recent studies have shed light on the influence of insect viruses on the competence of insect vectors for arboviruses. In this review, we focus on the biological effects of insect viruses on the transmission of arboviruses by insects. We also discuss the potential mechanisms by which insect viruses affect the ability of hosts to transmit arboviruses, as well as potential strategies for disease control through manipulation of insect viruses. Analyses of the interactions among insect vectors, insect viruses and arboviruses will provide new opportunities for development of innovative strategies to control arbovirus transmission.

Keywords

arbovirus / insect biology / insect vectors / insect virus / interaction / transmission

Cite this article

Download citation ▾
Hui Wang, Qian Chen, Taiyun Wei. Complex interactions among insect viruses-insect vector-arboviruses. Insect Science, 2024, 31(3): 683‒693 https://doi.org/10.1111/1744-7917.13285

References

[1]
Agboli,E., Leggewie, M., Altinli,M. and Schnettler,E. (2019) Mosquito specific viruses-transmission and interaction. Viruses, 11, 873.
[2]
Altinli,M., Schnettler, E. and Sicard,M. (2021) Symbiotic interactions between mosquitoes and mosquito viruses. Frontiers in Cellular and Infection Microbiology, 11, 694020.
[3]
An,X., Gu,Q., Wang,J., Chang, T., Zhang,W., Wang,J.J. et al. (2023) Insect-specific RNA virus affects the stylet penetration activity of brown citrus aphid (Aphis citricidus) to facilitate its transmission. Insect Science. Available from: PMID: 37358052.
CrossRef Google scholar
[4]
Baidaliuk,A., Miot,E.F., Lequime,S., Moltini-Conclois, I., Delaigue,F., Dabo,S. et al. (2019) Cell-fusing agent virus reduces arbovirus dissemination in Aedes aegypti mosquitoes in vivo. Journal of Virology, 93, e00705–e00719.
[5]
Bolling,B.G., Weaver, S.C., Tesh,R.B. and Vasilakis,N. (2015) Insect-specific virus discovery: significance for the arbovirus community. Viruses, 7, 4911–4928.
[6]
Campos,S.S., Fernandes, R.S., Dos Santos,A.A.C., de Miranda,R.M., Telleria, E.L., Ferreira-de-Brito,A. et al. (2017) Zika virus can be venereally transmitted between Aedes aegypti mosquitoes. Parasite Vector, 10, 605.
[7]
Carvalho,V.L. and Long, M.T. (2021) Insect-specific viruses: an overview and their relationship to arboviruses of concern to humans and animals. Virology, 557, 34–43.
[8]
Chen,B., Chen,Y., Chen,H.Z., Liang, Z.Y., Chen,J.H., Wu,R.F. et al. (2023a) Identification, characterization and prevalence in southern China of a new iflavirus in the leafhopper Recilia dorsalis (Hemiptera: Cicadellidae). Virus Research, 323, 199005.
[9]
Chen,Q., Godfrey, K., Liu,J., Mao,Q., Kuo,Y.W. and Falk,B.W. (2019) A nonstructural protein responsible for viral spread of a novel insect reovirus provides a safe channel for biparental virus transmission to progeny. Journal of Virology, 93, e00702–e00719.
[10]
Chen,Q., Nouri,S., Zhang,Y., Erickson, A. and Falk,B.W. (2020) Diaphorina citri reovirus is most closely related to fijiviruses. Virology, 547, 20–26.
[11]
Chen,Q., Zhang,Y., Yang,H., Wang, X., Ren,J., Jia,D. et al. (2023b) GAPDH mediates plant reovirus-induced incomplete autophagy for persistent viral infection in leafhopper vector. Autophagy, 19, 1100–1113.
[12]
Chen,Y., Lu,C., Li,M., Wu, W., Zhou,G. and Wei,T. (2016) Adverse effects of rice gall dwarf virus upon its insect vector Recilia dorsalis (Hemiptera: Cicadellidae). Plant Disease, 100, 784–790.
[13]
Fu,Y., Cao,M., Wang,H., Du, Z., Liu,Y. and Wang,X. (2020) Discovery and characterization of a novel insect-specific reovirus isolated from Psammotettix alienus. Journal of General Virology, 101, 884–892.
[14]
Goenaga,S., Kenney, J.L., Duggal,N.K., Delorey,M., Ebel,G.D., Zhang,B. et al. (2015) Potential for co-infection of a mosquito-specific flavivirus, Nhumirim virus, to block West Nile virus transmission in mosquitoes. Viruses, 7, 5801–5812.
[15]
Gray,S., Cilia,M. and Ghanim,M. (2014) Circulative, “nonpropagative” virus transmission: an orchestra of virus-, insect-, and plant-derived instruments. Advances in Virus Research, 89, 41–99.
[16]
Hall-Mendelin,S., McLean, B.J., Bielefeldt-Ohmann,H., Hobson-Peters,J., Hall,R.A., van den Hurk, A.F. et al. (2016) The insect-specific Palm Creek virus modulates West Nile virus infection in and transmission by Australian mosquitoes. Parasites Vectors, 9, 414.
[17]
Hobson-Peters,J., Yam, A.W., Lu,J.W., Setoh,Y.X., May,F.J., Kurucz,N. et al. (2013) A new insect-specific flavivirus from northern Australia suppresses replication of West Nile virus and Murray Valley encephalitis virus in co-infected mosquito cells. PLoS ONE, 8, e56534.
[18]
Hogenhout,S.A., Ammar,E.-D., Whitfield,A.E. and Redinbaugh,M.G. (2008) Insect vector interactions with persistently transmitted viruses. Annual Review of Phytopathology, 46, 327–359.
[19]
Huang,H.J., Ye,Z.X., Wang,X., Yan, X.T., Zhang,Y., He,Y.J. et al. (2021) Diversity and infectivity of the RNA virome among different cryptic species of an agriculturally important insect vector: whitefly Bemisia tabaci. NPJ Biofilms and Microbiomes, 7, 43.
[20]
Jia,D., Luo,G., Shi,W., Liu, Y., Liu,H., Zhang,X. et al. (2022a) Rice gall dwarf virus promotes the propagation and transmission of rice stripe mosaic virus by co-infected insect vectors. Frontiers in Microbiology, 13, 834712.
[21]
Jia,D., Liang,Q., Liu,H., Li, G., Zhang,X., Chen,Q. et al. (2022b) A nonstructural protein encoded by a rice reovirus induces an incomplete autophagy to promote viral spread in insect vectors. PLoS Pathogens, 18, e1010506.
[22]
Jia,D., Liang,Q., Chen,H., Liu, H., Li,G., Zhang,X. et al. (2023) Autophagy mediates a direct synergistic interaction during co-transmission of two distinct arboviruses by insect vectors. Science China Life Sciences, 66, 1665–1681.
[23]
Jia,W., Wang,F., Li,J., Chang, X., Yang,Y., Yao,H. et al. (2021) A novel iflavirus was discovered in green rice leafhopper Nephotettix cincticeps and its proliferation was inhibited by infection of rice dwarf virus. Frontiers in Microbiology, 11, 621141.
[24]
Käfer,S., Paraskevopoulou, S., Zirkel,F., Wieseke,N., Donath, A., Petersen,M. et al. (2019) Reassessing the diversity of negative strand RNA viruses in insects. PLoS Pathogens, 15, e1008224
[25]
Kenney,J.L. Solberg, O.D., Langevin,S.A. and Brault,A.C. (2014) Characterization of a novel insect-specific flavivirus from Brazil: potential for inhibition of infection of arthropod cells with medically important flaviviruses. Journal of General Virology, 95, 2796–2808.
[26]
Khine,M.O., Wang,H., Raza,A., Liu, Y. and Wang,X. (2020) The complete genomic sequence of a new iflavirus from the leafhopper Psammotettix alienus. Archives of Virology, 165, 1883–1886.
[27]
Lan,H., Wang,H., Chen,Q., Chen, H., Jia,D., Mao,Q. et al. (2016a) Small interfering RNA pathway modulates persistent infection of a plant virus in its insect vector. Scientific Reports, 6, 20699.
[28]
Lan,H., Chen,H., Liu,Y., Jiang, C., Mao,Q., Jia,D. et al. (2016b) Small interfering RNA pathway modulates initial viral infection in midgut epithelium of insect after ingestion of virus. Journal of Virology, 90, 917–929.
[29]
Leta,S., Beyene, T.J., De Clercq,E.M., Amenu,K., Kraemer, M.U.G. and Revie,C.W. (2018) Global risk mapping for major diseases transmitted by Aedes aegypti and Aedes albopictus. International Journal of Infectious Diseases, 67, 25–35.
[30]
Li,C.X., Shi,M., Tian,J.H., Lin, X.D., Kang,Y.J., Chen,L.J. et al. (2015a) Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. eLife, 4, e05378.
[31]
Li,J., Andika, I.B., Shen,J., Lv,Y., Ji,Y., Sun,L. et al. (2013) Characterization of rice black-streaked dwarf virus-and rice stripe virus derived siRNAs in singly and doubly infected insect vector Laodelphax striatellus. PLoS ONE, 8, e66007.
[32]
Li,T., Li,H., Wu,Y., Li, S., Yuan,G. and Xu,P. (2022) Identification of a novel densovirus in aphid, and uncovering the possible antiviral process during its infection. Frontiers in Immunology, 13, 905628.
[33]
Li,S., Ge,S., Wang,X., Sun, L., Liu,Z. and Zhou,Y. (2015b) Facilitation of rice stripe virus accumulation in the insect vector by Himetobi P virus VP1. Viruses, 7, 1492–1504.
[34]
Liu,W., Hajano, J.U. and Wang,X. (2018) New insights on the transmission mechanism of tenuiviruses by their vector insects. Current Opinion in Virology, 33, 13–17.
[35]
Lu,G., Zhang,X.D., Xu,Z.T., Ye, Z.X., Zhang,Y., Chen,J.P. et al. (2022) Complete sequence and genetic characterization of a novel insect-specific reovirus discovered from Laodelphax striatellus. Virology, 570, 117–122.
[36]
Lu,H., Zhu,J., Yu,J., Chen, X., Kang,L. and Cui,F. (2020) A symbiotic virus facilitates aphid adaptation to host plants by suppressing jasmonic acid responses. Molecular Plant-Microbe Interactions: MPMI, 33, 55–65.
[37]
Ma,E., Zhu,Y., Liu,Z., Wei, T., Wang,P. and Cheng,G. (2021) Interaction of viruses with the insect intestine. Annual Review of Virology, 8, 115–131.
[38]
Ma,R., Nie,B., Chen,J., Lv, K., Xiao,J. and Liu,R. (2022) Full genome sequence of a novel iflavirus from the leafhopper Recilia dorsalis. Archives of Virology, 167, 1593–1596.
[39]
Mao,Q., Wu,W., Liao,Z., Li, J., Jia,D., Zhang,X. et al. (2019) Viral pathogens hitchhike with insect sperm for paternal transmission. Nature Communications, 10, 955.
[40]
Murakami,R., Suetsugu, Y. and Nakashima,N. (2014) Complete genome sequences of two iflaviruses from the brown planthopper, Nilaparvata lugens. Archives of Virology, 159, 585–588.
[41]
Moya Fernández,M.B., Liu,W., Zhang,L., Hajano,J.U.D. and Wang,X. (2021) Interplay of rice stripe virus and rice black streaked dwarf virus during their acquisition and accumulation in insect vector. Viruses, 13, 1121.
[42]
Nakashima,N. and Noda, H. (1995) Nonpathogenic Nilaparvata lugens reovirus is transmitted to the brown planthopper through rice plant. Virology, 207, 303–307.
[43]
Nasar,F. Gorchakov, R.V., Tesh,R.B. and Weaver,S.C. (2015) Eilat virus induces both homologous and heterologous interference. Virology, 484, 51–58.
[44]
Nouri,S., Salem,N., Nigg,J.C. and Falk, B.W. (2016) Diverse array of new viral sequences identified in worldwide populations of the Asian citrus psyllid (Diaphorina citri) using viral metagenomics. Journal of Virology, 90, 2434–2445.
[45]
Öhlund,P., Lunden, H. and Blomstrom,A.L. (2019) Insect-specific virus evolution and potential effects on vector competence. Virus Genes, 55, 127–137.
[46]
Olmo,R.P., Todjro, Y.M.H., Aguiar,E.R.G.R. de Almeida,J.P.P., Ferreira, F.V., Armache,J.N. et al. (2023) Mosquito vector competence for dengue is modulated by insect-specific viruses. Nature Microbiology, 8, 135–149.
[47]
Patterson,E.I., Villinger, J., Muthoni,J.N., Dobel-Ober,L. and Hughes, G.L. (2020) Exploiting insect-specific viruses as a novel strategy to control vector -borne disease. Current Opinion in Insect Science, 39, 50–56.
[48]
Palmer,W.H., Medd,N.C., Beard,P.M. and Obbard, D.J. (2018) Isolation of a natural DNA virus of Drosophila melanogaster, and characterisation of host resistance and immune responses. PLoS Pathogens, 14, e1007050.
[49]
Romo,H., Kenney, J.L., Blitvich,B.J. and Brault,A.C. (2018) Restriction of Zika virus infection and transmission in Aedes aegypti mediated by an insect-specific flavivirus. Emerging Microbes & Infections, 7, 181.
[50]
Schultz,M.J., Frydman, H.M. and Connor,J.H. (2018) Dual Insect specific virus infection limits Arbovirus replication in Aedes mosquito cells. Virology, 518, 406–413.
[51]
Shi,M., Lin,X.D., Tian,J.H., Chen, L.J., Chen,X., Li,C.X. et al. (2016) Redefining the invertebrate RNA virosphere. Nature, 540, 539–543.
[52]
Tan,C.W., Peiffer, M., Hoover,K., Rosa,C., Acevedo, F.E. and Felton,G.W. (2018) Symbiotic polydnavirus of a parasite manipulates caterpillar and plant immunity. Proceedings of the National Academy of Sciences USA, 115, 5199–5204.
[53]
Thompson,W.H. and Beaty, B.J. (1977) Venereal transmission of La Crosse (California encephalitis) arbovirus in Aedes triseriatus mosquitoes. Science, 196, 530–531.
[54]
Thompson,W.H. and Beaty, B.J. (1978) Venereal transmission of La Crosse virus from male to female Aedes triseriatus. American Journal of Tropical Medicine and Hygiene, 27, 187–196.
[55]
Vasilakis,N. and Tesh, R.B. (2015) Insect-specific viruses and their potential impact on arbovirus transmission. Current Opinion in Virology, 15, 69–74.
[56]
Wan,G., Jiang,S., Wang,W., Li, G., Tao,X., Pan,W. et al. (2015) Rice stripe virus counters reduced fecundity in its insect vector by modifying insect physiology, primary endosymbionts and feeding behavior. Scientific Reports, 5, 12527.
[57]
Wan,J., Liang,Q., Zhang,R., Cheng, Y., Wang,X., Wang,H. et al. (2023) Arboviruses and symbiotic viruses cooperatively hijack insect sperm-specific proteins for paternal transmission. Nature Communications, 14, 1289.
[58]
Wang,F., Fang,Q., Wang,B., Yan, Z., Hong,J., Bao,Y. et al. (2017a) A novel negative-stranded RNA virus mediates sex ratio in its parasitoid host. PLoS Pathogens, 13, e1006201.
[59]
Wang,H., Liu,Y., Liu,W., Cao, M. and Wang,X. (2019a) Full genome sequence of a novel iflavirus from the leafhopper Psammotettix alienus. Archives of Virology, 164, 309–311.
[60]
Wang,H., Liu,Y., Liu,W., Cao, M. and Wang,X. (2019b) Sequence analysis and genomic organization of a novel chuvirus, Tàiyuán leafhopper virus. Archives of Virology, 164, 617–620.
[61]
Wang,H., Liu,Y., Liu,W., Wu, K. and Wang,X. (2022a) F-actin dynamics in midgut cells enables virus persistence in vector insects. Molecular Plant Pathology, 23, 1671–1685.
[62]
Wang,Y., Mao,Q., Liu,W., Mar, T., Wei,T., Liu,Y. et al. (2014) Localization and distribution of wheat dwarf virus in its vector leafhopper, Psammotettix alienus. Phytopathology, 104, 897–904.
[63]
Wang,Y.M., He,Y.Z., Ye,X.T., Guo, T., Pan,L.L., Liu,S.S. et al. (2022b) A balance between vector survival and virus transmission is achieved through JAK/STAT signaling inhibition by a plant virus. Proceedings of the National Academy of Sciences USA, 119, e2122099119.
[64]
Wang,W., Zhao,W., Li,J., Luo, L., Kang,L. and Cui,F. (2017b) The c-Jun N-terminal kinase pathway of a vector insect is activated by virus capsid protein and promotes viral replication. eLife, 6, e26591.
[65]
Wei,T. and Li,Y. (2016) Rice reoviruses in insect vectors. Annual Review of Phytopathology, 54, 99–120.
[66]
Wu,N., Zhang,P., Liu,W., Cao, M., Massart,S. and Wang,X. (2019) Complete genome sequence and characterization of a new iflavirus from the small brown planthopper (Laodelphax striatellus). Virus Research, 272, 197651.
[67]
Xiao,Y., Li,W., Yang,X., Xu, P., Jin,M., Yuan,H. et al. (2021) Rapid spread of a densovirus in a major crop pest following wide-scale adoption of Bt-cotton in China. eLife, 10, e66913.
[68]
Xu,H., He,X., Zheng,X., Yang, Y., Tian,J. and Lu,Z. (2014a) Southern rice blackstreaked dwarf virus (SRBSDV) directly affects the feeding and reproduction behavior of its vector, Sogatella furcifera (Horvath) (Hemiptera: Delphacidae). Virology, 11, 55.
[69]
Xu,P., Liu,Y., Graham,R.I., Wilson, K. and Wu,K. (2014b) Densovirus is a mutualistic symbiont of a global crop pest (Helicoverpa armigera) and protects against a baculovirus and Bt biopesticide. PLoS Pathogens, 10, e1004490.
[70]
Xu,P., Yang,L., Yang,X., Li, T., Graham,R.I., Wu,K. et al. (2020) Novel partiti-like viruses are conditional mutualistic symbionts in their normal lepidopteran host, African armyworm, but parasitic in a novel host, Fall armyworm. PLoS Pathogens, 16, e1008467.
[71]
Xu,Y., Huang,L., Wang,Z., Fu, S., Che,J., Qian,Y. et al. (2014c) Identification of Himetobi P virus in the small brown planthopper by deep sequencing and assembly of virus-derived small interfering RNAs. Virus Research, 179, 235–240.
[72]
Yang,X., Xu,P., Yuan,H., Graham, R.I., Wilson,K. and Wu,K. (2019) Discovery and characterization of a novel picorna-like RNA virus in the cotton bollworm Helicoverpa armigera. Journal of Invertebrate Pathology, 160, 1–7.
[73]
Zhao,P., Sun,X., Li,P., Sun, J., Yue,Y., Wei,J. et al. (2019) Infection characteristics of rice stripe mosaic virus in the body of the vector leafhoppers. Frontiers in Microbiology, 9, 3258.
[74]
Zhang,J., Wang,F., Yuan,B., Yang, L., Yang,Y., Fang,Q. et al. (2021) A novel cripavirus of an ectoparasitoid wasp increases pupal duration and fecundity of the wasp's Drosophila melanogaster host. The ISME Journal, 15, 3239–3257.
[75]
Zhang,L., Liu,W., Wu,N., Wang, H., Zhang,Z., Liu,Y. et al. (2023a) Southern rice black-streaked dwarf virus induces incomplete autophagy for persistence in gut epithelial cells of its vector insect. PLoS Pathogens, 19, e1011134.
[76]
Zhang,Y., Li,B.X., Mao,Q.Z., Zhuo, J.C., Huang,H.J., Lu,J.B. et al. (2023b) The JAK-STAT pathway promotes persistent viral infection by activating apoptosis in insect vectors. PLoS Pathogens, 19, e1011266.

RIGHTS & PERMISSIONS

2023 2023 The Authors. Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.
PDF

Accesses

Citations

Detail

Sections
Recommended

/