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Research Paper

Rhabdovirus encoded glycoprotein induces and harnesses host antiviral autophagy for maintaining its compatible infection

, , , , , , , , , , , , , , , , , , , , & ORCID Icon show all
Pages 275-294 | Received 09 Feb 2023, Accepted 21 Aug 2023, Published online: 01 Sep 2023
 

ABSTRACT

Macroautophagy/autophagy has been recognized as a central antiviral defense mechanism in plant, which involves complex interactions between viral proteins and host factors. Rhabdoviruses are single-stranded RNA viruses, and the infection causes serious harm to public health, livestock, and crop production. However, little is known about the role of autophagy in the defense against rhabdovirus infection by plant. In this work, we showed that Rice stripe mosaic cytorhabdovirus(RSMV) activated autophagy in plants and that autophagy served as an indispensable defense mechanism during RSMV infection. We identified RSMV glycoprotein as an autophagy inducer that interacted with OsSnRK1B and promoted the kinase activity of OsSnRK1B on OsATG6b. RSMV glycoprotein was toxic to rice cells and its targeted degradation by OsATG6b-mediated autophagy was essential to restrict the viral titer in plants. Importantly, SnRK1-glycoprotein and ATG6-glycoprotein interactions were well-conserved between several other rhabdoviruses and plants. Together, our data support a model that SnRK1 senses rhabdovirus glycoprotein for autophagy initiation, while ATG6 mediates targeted degradation of viral glycoprotein. This conserved mechanism ensures compatible infection by limiting the toxicity of viral glycoprotein and restricting the infection of rhabdoviruses.

Abbreviations: AMPK: adenosine 5‘-monophosphate (AMP)-activated protein kinase; ANOVA: analysis of variance; ATG: autophagy related; AZD: AZD8055; BiFC: bimolecular fluorescence complementation; BYSMV: barley yellow striate mosaic virus; Co-IP: co-immunoprecipitation; ConA: concanamycin A; CTD: C-terminal domain; DEX: dexamethasone; DMSO: dimethyl sulfoxide; G: glycoprotein; GFP: green fluorescent protein; MD: middle domain; MDC: monodansylcadaverine; NTD: N-terminal domain; OE: over expression; Os: Oryza sativa; PBS: phosphate-buffered saline; PtdIns3K: class III phosphatidylinositol-3-kinase; qRT-PCR: quantitative real-time reverse-transcription PCR; RFP: red fluorescent protein; RSMV: rice stripe mosaic virus; RSV: rice stripe virus; SGS3: suppressor of gene silencing 3; SnRK1: sucrose nonfermenting1-related protein kinase1; SYNV: sonchus yellow net virus; TEM: transmission electron microscopy; TM: transmembrane region; TOR: target of rapamycin; TRV: tobacco rattle virus; TYMaV: tomato yellow mottle-associated virus; VSV: vesicular stomatitis virus; WT: wild type; Y2H: yeast two-hybrid; YFP: yellow fluorescent protein.

Acknowledgements

We thank Prof. Jianxiang Wu (Zhejiang University, Hangzhou, China) for providing RSMV nucleocapsid protein specific antibody; Prof. Zhenghe Li (Zhejiang University, Hangzhou, China) for providing the SYNV-GFP and the plasmids containing the glycoprotein coding sequences of SYNV and TYMaV; Prof. Xianbing Wang (China Agricultural University, Beijing, China) for providing the plasmids containing the glycoprotein coding sequence of BYSMV; Prof. Fangfang Li (Institute of Plant Protection, Chinese Academy of Agricultural Sciences) for providing the constructed pTRV2 and YFP-NbATG8a plasmids. No conflict of interest declared.

Disclosure statement

No potential conflict of interest was reported by the authors.

Supplementary Material

Supplemental data for this article can be accessed here

Correction Statement

This article has been corrected with minor changes. These changes do not impact the academic content of the article.

Additional information

Funding

This work was supported by the grants from the National Natural Science Foundation of China (32072388, 32222071), Guangdong Special Branch Plan for Young Talent with Scientific and Technological Innovation (2019TQ05N158), Natural Science Foundation of Guangdong Province (2022A1515010770), the Postdoctoral Science Foundation of China (2021M691083), Science and Technology Base and Talent Special Project of Guangxi Province (GuikeAD22035012), and Guangdong Provincial Innovation Team for General Key Technologies in Modern Agricultural Industry (2019KJ133).

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