State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China.
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou, China.
Mol Plant Pathol. 2022 Nov;23(11):1671-1685. doi: 10.1111/mpp.13260. Epub 2022 Sep 8.
Hemipteran insects that transmit plant viruses in a persistent circulative manner acquire, retain and transmit viruses for their entire life. The mechanism enabling this persistence has remained unclear for many years. Here, we determined how wheat dwarf virus (WDV) persists in its leafhopper vector Psammotettix alienus. We found that WDV caused the up-regulation of actin-depolymerizing factor (ADF) at the mRNA and protein levels in the midgut cells of leafhoppers after experiencing a WDV acquisition access period (AAP) of 6, 12 or 24 h. Experimental inhibition of F-actin depolymerization by jasplakinolide and dsRNA injection led to lower virus accumulation levels and transmission efficiencies, suggesting that depolymerization of F-actin regulated by ADF is essential for WDV invasion of midgut cells. Exogenous viral capsid protein (CP) inhibited ADF depolymerization of actin filaments in vitro and in Spodoptera frugiperda 9 (Sf9) cells because the CP competed with actin to bind ADF and then blocked actin filament disassembly. Interestingly, virions colocalized with ADF after a 24-h AAP, just as actin polymerization occurred, indicating that the binding of CP with ADF affects the ability of ADF to depolymerize F-actin, inhibiting WDV entry. Similarly, the luteovirus barley yellow dwarf virus also induced F-actin depolymerization and then polymerization in the gut cells of its vector Schizaphis graminum. Thus, F-actin dynamics are altered by nonpropagative viruses in midgut cells to enable virus persistence in vector insects.
以持久循环方式传播植物病毒的半翅目昆虫在其整个生命周期中获取、保留和传播病毒。多年来，使这种持久性成为可能的机制仍不清楚。在这里，我们确定了小麦矮化病毒（WDV）如何在其叶蝉载体 Psammotettix alienus 中持续存在。我们发现，WDV 导致叶蝉中肠细胞的肌动蛋白解聚因子（ADF）在经历 6、12 或 24 小时的 WDV 获得访问期（AAP）后，在 mRNA 和蛋白质水平上调。实验抑制 jasplakinolide 和 dsRNA 注射引起的 F-actin 解聚导致病毒积累水平和传播效率降低，表明 ADF 调节的 F-actin 解聚对于 WDV 入侵中肠细胞是必不可少的。外源性病毒衣壳蛋白（CP）在体外和 Spodoptera frugiperda 9（Sf9）细胞中抑制肌动蛋白丝的 ADF 解聚，因为 CP 与肌动蛋白竞争与 ADF 结合，然后阻止肌动蛋白丝的解体。有趣的是，在 24 小时的 AAP 后，病毒粒子与 ADF 共定位，就像肌动蛋白聚合一样，表明 CP 与 ADF 的结合会影响 ADF 解聚 F-actin 的能力，从而抑制 WDV 的进入。同样，杆状病毒大麦黄矮病毒也诱导其载体禾谷缢管蚜肠道细胞中的 F-actin 解聚，然后聚合。因此，非增殖性病毒会改变中肠细胞中的 F-actin 动力学，从而使病毒在载体昆虫中持续存在。
