Fibrillar structures induced by a plant reovirus target mitochondria to activate typical apoptotic response and promote viral infection in insect vectors

文献类型： 外文期刊

第一作者： Zheng, Limin

作者： Zheng, Limin;Mao, Qianzhuo;Liu, Jiejie;Wang, Haitao;Jia, Dongsheng;Chen, Hongyan;Wu, Wei;Wei, Taiyun;Zheng, Limin

作者机构：

期刊名称：PLOS PATHOGENS （ 影响因子：6.823； 五年影响因子：7.455 ）

ISSN： 1553-7366

年卷期： 2019 年 15 卷 1 期

页码：

收录情况： SCI

摘要： Numerous plant viruses that cause significant agricultural problems are persistently transmitted by insect vectors. We wanted to see if apoptosis was involved in viral infection process in the vector. We found that a plant reovirus (rice gall dwarf virus, RGDV) induced typical apoptotic response during viral replication in the leafhopper vector and cultured vector cells, as demonstrated by mitochondrial degeneration and membrane potential decrease. Fibrillar structures formed by nonstructural protein Pns11 of RGDV targeted the outer membrane of mitochondria, likely by interaction with an apoptosis-related mitochondrial protein in virus-infected leafhopper cells or nonvector insect cells. Such association of virus-induced fibrillar structures with mitochondria clearly led to mitochondrial degeneration and membrane potential decrease, suggesting that RGDV Pns11 was the inducer of apoptotic response in insect vectors. A caspase inhibitor treatment and knockdown of caspase gene expression using RNA interference each reduced apoptosis and viral accumulation, while the knockdown of gene expression for the inhibitor of apoptosis protein improved apoptosis and viral accumulation. Thus, RGDV exploited caspase-dependent apoptotic response to promote viral infection in insect vectors. For the first time, we directly confirmed that a nonstructural protein encoded by a persistent plant virus can induce the typical apoptotic response to benefit viral transmission by insect vectors. Author summary Of the approximately 700 known plant viruses, more than 75% are transmitted by insects. Numerous plant viruses can replicate inside the cells of the insects. Unlike in the plant hosts, the viruses do not seem to cause disease in the insect vectors that carry them. Here, we report that the replication of a plant reovirus, rice gall dwarf virus (RGDV), activated the apoptotic response in limited areas of leafhopper vectors during viral replication. Interestingly, fibrillar structures constituted by nonstructural protein Pns11, which is encoded by RGDV, targeted the mitochondria and induced apoptotic response in the absence of viral replication, possibly via the specific interaction of RGDV Pns11 with an apoptosis-related mitochondrial outer membrane-associated protein. Our findings further suggest that the activation of apoptotic response facilitates efficient viral infection, whereas inhibition of apoptotic response blocks viral infection in insect vectors. This work presents a novel discovery that a plant reovirus induces typical apoptotic response and thus promotes its transmission by insect vectors.

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