Arboviruses antagonize insect Toll antiviral immune signaling to facilitate the coexistence of viruses with their vectors.

Many plant arboviruses are persistently transmitted by piercing-sucking insect vectors. However, it remains largely unknown how conserved insect Toll immune response exerts antiviral activity and how plant viruses antagonize it to facilitate persistent viral transmission. Here, we discover that southern rice black-streaked dwarf virus (SRBSDV), a devastating planthopper-transmitted rice reovirus, activates the upstream Toll receptors expression but suppresses the downstream MyD88-Dorsal-defensin cascade, resulting in the attenuation of insect Toll immune response. Toll pathway-induced the small antibacterial peptide defensin directly interacts with viral major outer capsid protein P10 and thus binds to viral particles, finally blocking effective viral infection in planthopper vector. Furthermore, viral tubular protein P7-1 directly interacts with and promotes RING E3 ubiquitin ligase-mediated ubiquitinated degradation of Toll pathway adaptor protein MyD88 through the 26 proteasome pathway, finally suppressing antiviral defensin production. This virus-mediated attenuation of Toll antiviral immune response to express antiviral defensin ensures persistent virus infection without causing evident fitness costs for the insects. E3 ubiquitin ligase also is directly involved in the assembly of virus-induced tubules constructed by P7-1 to facilitate viral spread in planthopper vector, thereby acting as a pro-viral factor. Together, we uncover a previously unknown mechanism used by plant arboviruses to suppress Toll immune response through the ubiquitinated degradation of the conserved adaptor protein MyD88, thereby facilitating the coexistence of arboviruses with their vectors in nature. Author summary: Many devastating plant viral pathogens are persistently transmitted by arthropod insects without causing evident insect fitness costs. However, how Toll pathway plays an antiviral role and how viruses antagonize Toll antiviral immune response are still poorly understood. Here, we report that the planthopper defensin, a type of antibacterial peptide induced by Toll pathway, directly binds to viral particles of an important rice reovirus, thus exerting antiviral activity. However, the virus-encoded protein promotes the ubiquitinated degradation of the conserved Toll pathway adaptor protein MyD88, finally suppressing defensin production. Such process finally ensures persistent virus transmission by insect vectors. Our findings provide insights into how viruses have evolved the novel strategies to evade and even exploit insect Toll antiviral immune response to facilitate persistent viral transmission. [ABSTRACT FROM AUTHOR]