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  3. A balance between vector survival and virus transmission is achieved through JAK/STAT signaling inhibition by a plant virus

A balance between vector survival and virus transmission is achieved through JAK/STAT signaling inhibition by a plant virus

  • Proc Natl Acad Sci U S A. 2022 Oct 11;119(41):e2122099119. doi: 10.1073/pnas.2122099119.
Yu-Meng Wang 1 2 3,  Ya-Zhou He 4 5,  Xin-Tong Ye 1 2 3,  Tao Guo 1 2 3,  Li-Long Pan 1 2 3,  Shu-Sheng Liu 1 2 3,  James C K Ng 6,  Xiao-Wei Wang 1 2 3
Affiliations

Affiliations

  • 1 State Key Laboratory of Rice Biology, Zhejiang University, Hangzhou, 310058 China.
  • 2 Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Zhejiang University, Hangzhou, 310058 China.
  • 3 Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Zhejiang University, Hangzhou, 310058 China.
  • 4 Key Laboratory of Integrated Pest Management on Crops in East China (MARA), Nanjing Agricultural University, Nanjing, 21095 China.
  • 5 College of Plant Protection, Nanjing Agricultural University, Nanjing, 21095 China.
  • 6 Department of Microbiology and Plant Pathology, University of California, Riverside, CA 92521.
PMID: 36191206 DOI: 10.1073/pnas.2122099119
Abstract

Viruses pose a great threat to animal and plant health worldwide, with many being dependent on insect vectors for transmission between hosts. While the virus-host arms race has been well established, how viruses and insect vectors adapt to each other remains poorly understood. Begomoviruses comprise the largest genus of plant-infecting DNA viruses and are exclusively transmitted by the whitefly Bemisia tabaci. Here, we show that the vector Janus kinase/signal transducer and activator of transcription (JAK/STAT) pathway plays an important role in mediating the adaptation between the begomovirus tomato yellow leaf curl virus (TYLCV) and whiteflies. We found that the JAK/STAT pathway in B. tabaci functions as an Antiviral mechanism against TYLCV Infection in whiteflies as evidenced by the increase in viral DNA and coat protein (CP) levels after inhibiting JAK/STAT signaling. Two STAT-activated effector genes, BtCD109-2 and BtCD109-3, mediate this anti-TYLCV activity. To counteract this vector immunity, TYLCV has evolved strategies that impair the whitefly JAK/STAT pathway. Infection of TYLCV is associated with a reduction of JAK/STAT pathway activity in whiteflies. Moreover, TYLCV CP binds to STAT and blocks its nuclear translocation, thus, abrogating the STAT-dependent transactivation of target genes. We further show that inhibition of the whitefly JAK/STAT pathway facilitates TYLCV transmission but reduces whitefly survival and fecundity, indicating that this JAK/STAT-dependent TYLCV-whitefly interaction plays an important role in keeping a balance between whitefly fitness and TYLCV transmission. This study reveals a mechanism of plant virus-insect vector coadaptation in relation to vector survival and virus transmission.

Keywords

JAK/STAT; begomovirus; insect vector; virus transmission; whitefly.

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