A plant virus attenuates the Toll immune pathway by degradation of Pellino to facilitate viral infection in insect vectors.

Many plant viruses are persistently transmitted by insect vectors. The viral antagonism of insect innate immune responses is a critical step in ensuring persistent viral infection. Recent studies have shown that the Toll immune pathway mediates the persistent and propagative transmission of rice stripe virus (RSV) in its insect vector (Laodelphax striatellus). However, whether other host factors are involved in the Toll pathway and how RSV counteracts the Toll immune response in L. striatellus remain unclear. Here, we reported that LsPellino also inhibited RSV infection in L. striatellus by interacting with LsTube and participating in the Toll immune pathway. In contrast, the viral nonstructural protein NS3 hijacked the suppressor of cytokine signaling 5 (LsSOCS5) to promote the degradation of LsPellino via the 26S proteasome pathway, thereby suppressing the Toll immune response. In summary, these findings demonstrate that RSV attenuates the Toll immune pathway by degradation of LsPellino to facilitate viral infection in insect vectors. Our research provides new insights into controlling the transmission of vector-borne viruses.

Importance: Plant virus diseases pose a serious threat to global crop production. Nearly half of the known plant viruses are persistently transmitted by insect vectors, and these plant viruses must counteract various innate immune responses to maintain persistent infection. Here, we uncover a novel counter-defense mechanism against Toll antiviral defense. Our research showed that LsPellino exerts antiviral function by interacting with LsTube and participating in the Toll immune pathway. To counteract this immunity, a plant virus, rice stripe virus, attenuates the Toll immune pathway and promotes viral infection by using viral nonstructural protein NS3 to mediate the degradation of LsPellino in its insect vector, Laodelphax striatellus. This study not only contributes to a better understanding of the arms race between viruses and insect vectors but also provides a new perspective for controlling the transmission of plant viruses.