Autophagy mediates a direct synergistic interaction during co-transmission of two distinct arboviruses by insect vectors

Multiple viral infections in insect vectors with synergistic effects are common in nature, but the underlying mechanism remains elusive. Here, we find that rice gall dwarf reovirus (RGDV) facilitates the transmission of rice stripe mosaic rhabdovirus (RSMV) by co-infected leafhopper vectors. RSMV nu...

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Bibliographic Details
Published in:Science China. Life sciences 2023-07, Vol.66 (7), p.1665-1681
Main Authors: Jia, Dongsheng, Liang, Qifu, Chen, Hongyan, Liu, Huan, Li, Guangjun, Zhang, Xiaofeng, Chen, Qian, Wang, Aiming, Wei, Taiyun
Format: Article
Language:English
Subjects:
Animals
Antiviral agents
Arboviruses
Autophagy
Biomedical and Life Sciences
Expression vectors
Hemiptera - metabolism
Insect Vectors
Life Sciences
Oryza - metabolism
Phagosomes
Plant virus diseases
Plant viruses
Reoviridae - metabolism
Research Paper
Viral Nonstructural Proteins - metabolism
Virions
Virus Replication
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Summary:Multiple viral infections in insect vectors with synergistic effects are common in nature, but the underlying mechanism remains elusive. Here, we find that rice gall dwarf reovirus (RGDV) facilitates the transmission of rice stripe mosaic rhabdovirus (RSMV) by co-infected leafhopper vectors. RSMV nucleoprotein (N) alone activates complete anti-viral autophagy, while RGDV nonstructural protein Pns11 alone induces pro-viral incomplete autophagy. In co-infected vectors, RSMV exploits Pns11-induced autophagosomes to assemble enveloped virions via N-Pns11-ATG5 interaction. Furthermore, RSMV could effectively propagate in Sf9 cells. Expression of Pns11 in Sf9 cells or leafhopper vectors causes the recruitment of N from the ER to Pns11-induced autophagosomes and inhibits N-induced complete autophagic flux, finally facilitating RSMV propagation. In summary, these results demonstrate a previously unappreciated role of autophagy in the regulation of the direct synergistic interaction during co-transmission of two distinct arboviruses by insect vectors and reveal the functional importance of virus-induced autophagosomes in rhabdovirus assembly.
ISSN:1674-7305
1869-1889
DOI:10.1007/s11427-022-2228-y