Manipulation of host-plant preference by virus-induced changes to its insect vector’s olfactory system

Plant viruses are known to indirectly manipulate insect vector behavior by altering host-plant phenotypes, yet the mechanisms by which they directly regulate vector behavior to enhance transmission remain poorly understood. Here, we reveal how the southern rice black-streaked dwarf virus (SRBSDV) reprograms the host preference of its planthopper vector, Sogatella furcifera, from infected to healthy rice plants by disrupting immune-olfactory crosstalk. We demonstrate that the SRBSDV-encoded P8 protein competitively binds to the S. furcifera Pelle kinase, a core component of the Toll signaling pathway, thereby inhibiting the phosphorylation and nuclear translocation of the transcription factor Dorsal-related immunity factor (DIF). This immune suppression downregulates the E-β-farnesene-responsive odorant receptor Or86 while upregulating the β-caryophyllene-responsive receptor Or127, shifting the olfactory preference of virus-carrying planthoppers toward uninfected plants. Knocking down Or86 or Or127 abolished this behavioral shift, reducing viral transmission rates in both plants and vectors. Our findings uncover a tripartite mechanism wherein a viral effector co-opts conserved immune signaling to rewire chemosensory perception in insect vectors, promoting virus spread. This work advances insight into the molecular arms race between viruses and vectors, offering novel targets for disrupting viral transmission in agricultural ecosystems.