A Negative Feedback Loop Compromises NMD-Mediated Virus Restriction by the Autophagy Pathway in Plants

文献类型： 外文期刊

第一作者： Chen, Yalin

作者： Chen, Yalin;Jia, Mingxuan;Ge, Linhao;Li, Zhaolei;He, Hao;Zhou, Xueping;Li, Fangfang;Zhou, Xueping

作者机构：

关键词： autophagic degradation; nonsense mediated RNA decay; SMG7; UPF3; virus restriction

期刊名称：ADVANCED SCIENCE （ 影响因子：14.3； 五年影响因子：16.3 ）

ISSN：

年卷期： 2024 年 11 卷 32 期

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收录情况： SCI

摘要： Nonsense-mediated decay (NMD) and autophagy play pivotal roles in restricting virus infection in plants. However, the interconnection between these two pathways in viral infections has not been explored. Here, it is shown that overexpression of NbSMG7 and NbUPF3 attenuates cucumber green mottle mosaic virus (CGMMV) infection by recognizing the viral internal termination codon and vice versa. NbSMG7 is subjected to autophagic degradation, which is executed by its interaction with one of the autophagy-related proteins, NbATG8i. Mutation of the ATG8 interacting motif (AIM) in NbSMG7 (SMG7mAIM1) abolishes the interaction and comprises its autophagic degradation. Silencing of NbSMG7 and NbATG8i, or NbUPF3 and NbATG8i, compared to silencing each gene individually, leads to more virus accumulations, but overexpression of NbSMG7 and NbATG8i fails to achieve more potent virus inhibition. When CGMMV is co-inoculated with NbSMG7mAIM1 or with NbUPF3, compared to co-inoculating with NbSMG7 in NbATG8i transgene plants, the inoculated plants exhibit milder viral phenotypes. These findings reveal that NMD-mediated virus inhibition is impaired by the autophagic degradation of SMG7 in a negative feedback loop, and a novel regulatory interplay between NMD and autophagy is uncovered, providing insights that are valuable in optimizing strategies to harness NMD and autophagy for combating viral infections. Nonsense-mediated RNA decay (NMD) factors SMG7 and UPF3 recognize viral specific RNA features to mediate viral RNA degradation for restricting virus infection. However, overexpression of SMG7 can induce autophagy, and ATG8i-mediated the autophagic degradation of SMG7 compromises the combined anti-viral effects of NMD and autophagy. This finding reveals that autophagy negatively regulates NMD, which can be exploited by invading virus. image

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