Maintenance of persistent transmission of a plant arbovirus in its insect vector mediated by the Toll-Dorsal immune pathway

Abstract

Throughout evolution, arboviruses have developed various strategies to counteract the host’s innate immune defenses to maintain persistent transmission. Recent studies have shown that, in addition to bacteria and fungi, the innate Toll-Dorsal immune system also plays an essential role in preventing viral infections in invertebrates. However, whether the classical Toll immune pathway is involved in maintaining the homeostatic process to ensure the persistent and propagative transmission of arboviruses in insect vectors remain unclear. In this study, we revealed that the transcription factor Dorsal is actively involved in the antiviral defense of an insect vector ( Laodelphax striatellus ) by regulating the target gene, zinc finger protein 708 ( LsZN708 ), which mediates downstream immune-related effectors against infection with the plant virus (Rice stripe virus, RSV). In contrast, an antidefense strategy involving the use of the nonstructural-protein (NS4) to antagonize host antiviral defense through competitive binding to Dorsal from the MSK2 kinase was employed by RSV; this competitive binding inhibited Dorsal phosphorylation and reduced the antiviral response of the host insect. Our study revealed the molecular mechanism through which Toll-Dorsal-ZN708 mediates the maintenance of an arbovirus homeostasis in insect vectors. Specifically, ZN708 is a newly documented zinc finger protein targeted by Dorsal that mediates the downstream antiviral response. This study will contribute to our understanding of the successful transmission and spread of arboviruses in plant or invertebrate hosts.

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

“…In general, the adaptor protein MyD88 recruits Tube and Pelle to form a complex, which dissociates Cactus from the complex of Cactus and Dorsal, thereby initiating the translocation of the transcription factor Dorsal into the nucleus for regulating the expression of AMPs [ 14 ]. Recent report shows that RSV can antagonize the Toll antiviral response in planthopper vectors through competitively binding to Dorsal [ 24 ]. Toll pathways in insects exert strong evolutionary pressure on viruses, and viral evasion of the Toll immune response may occur in a conserved manner [ 13 , 23 , 37 ].…”

“…The Toll pathway also plays an antiviral role during RSV infection in planthopper vector [ 8 ]. Recent report shows that RSV-encoded nonstructural protein NS4 could antagonize planthopper vector antiviral Toll immune response through competitively binding to the transcription factor Dorsal that mediates the downstream antiviral response [ 24 ]. However, how plant arboviruses antagonize Toll immune response to induce antiviral AMPs to ensure persistent virus transmission by insect vectors is still unknown.…”