Interaction of EXA1 and eIF4E family members facilitates potexvirus infection in Arabidopsis thaliana
Interaction of EXA1 and eIF4E family members facilitates potexvirus infection in Arabidopsis thaliana
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EXA1 和 eIF4E 家族成员的相互作用促进拟南芥中的 Potexvirus 感染
DOI：
10.1128/jvi.00221-23
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发表时间：
2023
影响因子：
5.4
通讯作者：
Yasuyuki Yamaji
中科院分区：
文献类型：
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作者：
Masanobu Nishikawa;Kosuke Katsu;Hiroaki Koinuma;Masayoshi Hashimoto;Yutaro Neriya;Juri Matsuyama;Toya Yamamoto;Masato Suzuki;Oki Matsumoto;Hidenori Matsui;Hirofumi Nakagami;Kensaku Maejima;Shigetou Namba;Yasuyuki Yamaji
植物病毒的成功感染依赖于许多寄主因素。关键寄主因子的缺乏导致植物隐性遗传病毒抗性。例如，在拟南芥中失去了对痘病毒积累至关重要的1(EXA1)，从而获得了对痘病毒的抗性。然而，EXA1如何协助痘病毒感染的分子机制在很大程度上仍然未知。先前的研究报道了水杨酸（SA）通路在eds1突变体中上调，并且在eds1依赖性效应物触发的免疫过程中，dexa1调节超敏反应相关的细胞死亡。在这里，我们发现exa1介导的病毒耐药性主要独立于SA和EDS1途径。我们证明arabidopsisexa1通过eIF4E结合基序（4EBM）与真核翻译起始因子4E （eIF4E）家族的三个成员eIF4E1、eIFiso4E和新型帽结合蛋白（nCBP）相互作用。EXA1突变体的表达恢复了车前草花叶病毒（PlAMV）的感染，而EXA1突变体的表达仅部分恢复了车前草花叶病毒的感染。在拟南芥敲除突变体的病毒接种实验中，EXA1与nCBP协同促进PlAMV感染，但eIFiso4E和nCBP促进PlAMV感染的功能是多余的。相比之下，eIF4E1对PlAMV感染的促进作用至少部分与EXA1无关。综上所述，我们的结果表明EXA1-eIF4E家族成员的相互作用对PlAMV的有效增殖至关重要，尽管三个eIF4E家族成员在PlAMV感染中的具体作用不同。马铃薯病毒属包括一组植物RNA病毒，其中包括对农作物造成严重损害的病毒。我们之前的研究表明，拟南芥中缺失的poteXvirus Accumulation essential 1（EXA1）赋予了对poteXvirus的抗性。因此，EXA1可能在成功感染痘病毒中发挥关键作用；因此，阐明其作用机制对了解痘病毒的感染过程和有效控制病毒具有重要意义。先前的研究报道exa1的缺失增强了植物的免疫应答，但我们的研究结果表明这不是exa1介导的病毒抗性的主要机制。在这里，我们发现arabidopsisexa1通过与真核翻译启动因子4E家族相互作用，协助亚洲车前草花叶病毒（PlAMV）感染。我们的研究结果表明EXA1通过调节翻译来促进PlAMV的增殖。
Plant viruses depend on a number of host factors for successful infection. Deficiency of critical host factors confers recessively inherited viral resistance in plants. For example, loss ofEssential for poteXvirus Accumulation 1(EXA1) in Arabidopsis thaliana confers resistance to potexviruses. However, the molecular mechanism of how EXA1 assists potexvirus infection remains largely unknown. Previous studies reported that the salicylic acid (SA) pathway is upregulated inexa1mutants, andEXA1modulates hypersensitive response-related cell death during EDS1-dependent effector-triggered immunity. Here, we show thatexa1-mediated viral resistance is mostly independent of SA and EDS1 pathways. We demonstrate thatArabidopsisEXA1 interacts with three members of the eukaryotic translation initiation factor 4E (eIF4E) family, eIF4E1, eIFiso4E, and novel cap-binding protein (nCBP), through the eIF4E-binding motif (4EBM). Expression of EXA1 inexa1mutants restored infection by the potexvirusPlantago asiatica mosaic virus(PlAMV), but EXA1 with mutations in 4EBM only partially restored infection. In virus inoculation experiments usingArabidopsisknockout mutants, EXA1 promoted PlAMV infection in concert with nCBP, but the functions of eIFiso4E and nCBP in promoting PlAMV infection were redundant. By contrast, the promotion of PlAMV infection by eIF4E1 was, at least partially, EXA1 independent. Taken together, our results imply that the interaction of EXA1-eIF4E family members is essential for efficient PlAMV multiplication, although specific roles of three eIF4E family members in PlAMV infection differ.IMPORTANCEThe genusPotexviruscomprises a group of plant RNA viruses, including viruses that cause serious damage to agricultural crops. We previously showed that loss ofEssential for poteXvirus Accumulation 1(EXA1) in Arabidopsis thaliana confers resistance to potexviruses. EXA1 may thus play a critical role in the success of potexvirus infection; hence, elucidation of its mechanism of action is crucial for understanding the infection process of potexviruses and for effective viral control. Previous studies reported that loss ofEXA1enhances plant immune responses, but our results indicate that this is not the primary mechanism ofexa1-mediated viral resistance. Here, we show thatArabidopsisEXA1 assists infection by the potexvirusPlantago asiatica mosaic virus(PlAMV) by interacting with the eukaryotic translation initiation factor 4E family. Our results imply that EXA1 contributes to PlAMV multiplication by regulating translation.