Rice ragged stunt virus Pns10 induces mitochondrial-mediated apoptosis to promote viral infection in Nilaparvata lugens through disrupting the NlNDUFS1-NlPHB2 interaction.

Apoptosis, a programmed cell death process, plays crucial roles in host antiviral response. Although there are many reports on the relationship between cell apoptosis and viral infection, the mechanisms underlying plant arbovirus-induced apoptosis in insect vectors remain largely unclear. Here, we reported that apoptosis promotes rice ragged stunt virus (RRSV) infection in Nilaparvata lugens (brown planthopper), and RRSV-encoded Pns10 protein can induce apoptosis in N. lugens. The Pns10 interacts with N. lugens NADH:ubiquinone oxidoreductase 75 kDa Fe-S protein 1(NlNDUFS1), a core subunit of mitochondrial complex I. Silencing of NlNDUFS1 expression in N. lugens impaired mitochondrial complex I activity, decreasing ATP production and increasing mitochondrial ROS accumulation. This dysregulation triggers apoptosis to promote RRSV infection in N. lugens. Furthermore, RRSV Pns10 disrupts the interaction between NlNDUFS1 and NlProhibitin 2 (NlPHB2) in N. lugens to impair mitochondrial complex I activity, leading to a decrease of ATP production and an increase of mitochondrial ROS accumulation. The excessive accumulation of mitochondrial ROS causes genomic DNA fragmentation and apoptosis. Collectively, the findings presented here illuminate a novel mechanism by which a plant virus manipulates vector mitochondrial apoptosis to benefit viral infection, and offer insights for future transmission-blocking interventions.