Fujian Province Key Laboratory of Plant Virology, Vector-borne Virus Research Center, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou, Fujian, PR China.
PLoS Pathog. 2021 Mar 1;17(3):e1009347. doi: 10.1371/journal.ppat.1009347. eCollection 2021 Mar.
In the field, many insect-borne crop viral diseases are more suitable for maintenance and spread in hot-temperature areas, but the mechanism remains poorly understood. The epidemic of a planthopper (Sogatella furcifera)-transmitted rice reovirus (southern rice black-streaked dwarf virus, SRBSDV) is geographically restricted to southern China and northern Vietnam with year-round hot temperatures. Here, we reported that two factors of endoplasmic reticulum-associated degradation (ERAD) machinery, the heat shock protein DnaJB11 and ER membrane protein BAP31, were activated by viral infection to mediate the adaptation of S. furcifera to high temperatures. Infection and transmission efficiencies of SRBSDV by S. furcifera increased with the elevated temperatures. We observed that high temperature (35°C) was beneficial for the assembly of virus-containing tubular structures formed by nonstructural protein P7-1 of SRBSDV, which facilitates efficient viral transmission by S. furcifera. Both DnaJB11 and BAP31 competed to directly bind to the tubule protein P7-1 of SRBSDV; however, DnaJB11 promoted whereas BAP31 inhibited P7-1 tubule assembly at the ER membrane. Furthermore, the binding affinity of DnaJB11 with P7-1 was stronger than that of BAP31 with P7-1. We also revealed that BAP31 negatively regulated DnaJB11 expression through their direct interaction. High temperatures could significantly upregulate DnaJB11 expression but inhibit BAP31 expression, thereby strongly facilitating the assembly of abundant P7-1 tubules. Taken together, we showed that a new temperature-dependent protein quality control pathway in the ERAD machinery has evolved for strong activation of DnaJB11 for benefiting P7-1 tubules assembly to support efficient transmission of SRBSDV in high temperatures. We thus deduced that ERAD machinery has been hitchhiked by insect-borne crop viruses to enhance their transmission in tropical climates.
在田间，许多虫媒作物病毒病在高温地区更适合维持和传播，但机制仍不清楚。褐飞虱（Sogatella furcifera）传播的水稻呼肠孤病毒（南方水稻黑条矮缩病毒，SRBSDV）的流行仅限于中国南方和越南北部，那里全年气温较高。在这里，我们报道了内质网相关降解（ERAD）机制的两个因素，热休克蛋白 DnaJB11 和 ER 膜蛋白 BAP31，被病毒感染激活，介导褐飞虱适应高温。SRBSDV 对褐飞虱的感染和传播效率随着温度的升高而增加。我们观察到高温（35°C）有利于由 SRBSDV 的非结构蛋白 P7-1 形成的含有病毒的管状结构的组装，这有利于褐飞虱的高效病毒传播。DnaJB11 和 BAP31 都竞争与 SRBSDV 的管状蛋白 P7-1 直接结合；然而，DnaJB11 促进而 BAP31 抑制 ER 膜上 P7-1 管的组装。此外，DnaJB11 与 P7-1 的结合亲和力强于 BAP31 与 P7-1 的结合亲和力。我们还揭示了 BAP31 通过它们的直接相互作用负调控 DnaJB11 的表达。高温可以显著上调 DnaJB11 的表达，但抑制 BAP31 的表达，从而强烈促进大量 P7-1 管的组装。总之，我们表明，内质网中一种新的依赖温度的蛋白质质量控制途径在 ERAD 机制中进化而来，强烈激活 DnaJB11，有利于 P7-1 管的组装，从而支持 SRBSDV 在高温下的高效传播。因此，我们推断，内质网相关降解机制已被虫媒作物病毒搭便车，以增强其在热带气候下的传播。
