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

  • PLoS Pathog. 2025 Aug 19;21(8):e1013415. doi: 10.1371/journal.ppat.1013415.
Lianshun Zheng  1  2 ,  Shuai Fu  1  3 ,  Ming Zeng  1 ,  Liyan Li  1 ,  Dan Wang  1 ,  Shibo Gao  1 ,  Yunge Zhang  1 ,  Cui Zhang  1 ,  Shifang Fei  1  2 ,  Xuan Ye  1 ,  Lele Chen  1 ,  Qianhui Chen  1 ,  Yaqin Wang  1 ,  Xueping Zhou  1  4 ,  Yan Xie  1 ,  Boli Hu  5 ,  Jianxiang Wu  1  2
Affiliations
  • 1. State Key Laboratory of Rice Biology and Breeding, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang University, Hangzhou, Zhejiang, P.R. China.
  • 2. Hainan Institute of Zhejiang University, Sanya, P.R. China.
  • 3. Research Center for Life Sciences Computing, Zhejiang Lab, Hangzhou, China.
  • 4. State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, P.R. China.
  • 5. MOA Key Laboratory of Animal Virology, Zhejiang University Center for Veterinary Sciences, Hangzhou, P.R. China.
PMID: 40828869 DOI: 10.1371/journal.ppat.1013415
Abstract

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.

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