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

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Abstract

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.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31920103014, 31970160) and the Natural Science Foundation of Fujian Province (2020J06015). The antibodies Bip, ATG5, ATG8, Lamp1, and p62 were produced by Genscript USA Innovation Company (Nanjing), which is approved by the Science Technology Department of Jiangsu Province, China with approval number SYXK (Su) 2018-0015.

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Authors and Affiliations

  1. Vector-borne Virus Research Center, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou, 350002, China

    Dongsheng Jia, Qifu Liang, Hongyan Chen, Huan Liu, Guangjun Li, Xiaofeng Zhang, Qian Chen & Taiyun Wei

  2. London Research and Development Centre, Agriculture and Agri-Food Canada, London, Ontario, N5V 4T3, Canada

    Aiming Wang

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  1. Dongsheng Jia
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Correspondence to Taiyun Wei.

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

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Jia, D., Liang, Q., Chen, H. et al. Autophagy mediates a direct synergistic interaction during co-transmission of two distinct arboviruses by insect vectors. Sci. China Life Sci. 66, 1665–1681 (2023). https://doi.org/10.1007/s11427-022-2228-y

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