Viral proteins resolve the virus-vector conundrum during hemipteran-mediated transmission by subverting salicylic acid signaling pathway
Abstract Hemipteran insects transmit viruses when infesting plants, during which vectors activate salicylic acid (SA)-regulated antiviral defenses. How vector-borne plant viruses circumvent these antiviral defenses is largely unexplored. During co-infections of begomoviruses and betasatellites in pl...
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Nature Portfolio
2024-11-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-53894-y |
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| author | Jing-Ru Zhang Yi-Ming Liu Di Li Yi-Jie Wu Shi-Xing Zhao Xiao-Wei Wang Shu-Sheng Liu Linda L. Walling Li-Long Pan |
| author_facet | Jing-Ru Zhang Yi-Ming Liu Di Li Yi-Jie Wu Shi-Xing Zhao Xiao-Wei Wang Shu-Sheng Liu Linda L. Walling Li-Long Pan |
| author_sort | Jing-Ru Zhang |
| collection | DOAJ |
| description | Abstract Hemipteran insects transmit viruses when infesting plants, during which vectors activate salicylic acid (SA)-regulated antiviral defenses. How vector-borne plant viruses circumvent these antiviral defenses is largely unexplored. During co-infections of begomoviruses and betasatellites in plants, betasatellite-encoded βC1 proteins interfere with SA signaling and reduce the activation of antiviral resistance. βC1 inhibits SA-induced degradation of NbNPR3 (Nicotiana benthamiana nonexpressor of pathogenesis-related genes 3), a negative regulator of SA signaling. βC1 does not bind directly to NbNPR3, but regulates NbNPR3 degradation via heat shock protein 90s (NbHSP90s). NbHSP90s bind to both NbNPR3 and βC1 and suppress SA signaling. This viral success strategy appears to be conserved as it is also documented for viral proteins encoded by two aphid-borne viruses. Our findings reveal an exquisite mechanism that facilitates the persistence of vector-borne plant viruses and provide important insights into the intricacies of the virus life cycle. |
| format | Article |
| id | doaj-art-1a96f75efb5e4326a1cc6588ee4abecc |
| institution | OA Journals |
| issn | 2041-1723 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-1a96f75efb5e4326a1cc6588ee4abecc2025-08-20T02:18:28ZengNature PortfolioNature Communications2041-17232024-11-0115111710.1038/s41467-024-53894-yViral proteins resolve the virus-vector conundrum during hemipteran-mediated transmission by subverting salicylic acid signaling pathwayJing-Ru Zhang0Yi-Ming Liu1Di Li2Yi-Jie Wu3Shi-Xing Zhao4Xiao-Wei Wang5Shu-Sheng Liu6Linda L. Walling7Li-Long Pan8Ministry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang UniversityMinistry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang UniversityMinistry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang UniversityMinistry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang UniversityMinistry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang UniversityMinistry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang UniversityMinistry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang UniversityDepartment of Botany and Plant Sciences, Center for Plant Cell Biology, University of CaliforniaMinistry of Agriculture Key Lab of Molecular Biology of Crop Pathogens and Insects, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang UniversityAbstract Hemipteran insects transmit viruses when infesting plants, during which vectors activate salicylic acid (SA)-regulated antiviral defenses. How vector-borne plant viruses circumvent these antiviral defenses is largely unexplored. During co-infections of begomoviruses and betasatellites in plants, betasatellite-encoded βC1 proteins interfere with SA signaling and reduce the activation of antiviral resistance. βC1 inhibits SA-induced degradation of NbNPR3 (Nicotiana benthamiana nonexpressor of pathogenesis-related genes 3), a negative regulator of SA signaling. βC1 does not bind directly to NbNPR3, but regulates NbNPR3 degradation via heat shock protein 90s (NbHSP90s). NbHSP90s bind to both NbNPR3 and βC1 and suppress SA signaling. This viral success strategy appears to be conserved as it is also documented for viral proteins encoded by two aphid-borne viruses. Our findings reveal an exquisite mechanism that facilitates the persistence of vector-borne plant viruses and provide important insights into the intricacies of the virus life cycle.https://doi.org/10.1038/s41467-024-53894-y |
| spellingShingle | Jing-Ru Zhang Yi-Ming Liu Di Li Yi-Jie Wu Shi-Xing Zhao Xiao-Wei Wang Shu-Sheng Liu Linda L. Walling Li-Long Pan Viral proteins resolve the virus-vector conundrum during hemipteran-mediated transmission by subverting salicylic acid signaling pathway Nature Communications |
| title | Viral proteins resolve the virus-vector conundrum during hemipteran-mediated transmission by subverting salicylic acid signaling pathway |
| title_full | Viral proteins resolve the virus-vector conundrum during hemipteran-mediated transmission by subverting salicylic acid signaling pathway |
| title_fullStr | Viral proteins resolve the virus-vector conundrum during hemipteran-mediated transmission by subverting salicylic acid signaling pathway |
| title_full_unstemmed | Viral proteins resolve the virus-vector conundrum during hemipteran-mediated transmission by subverting salicylic acid signaling pathway |
| title_short | Viral proteins resolve the virus-vector conundrum during hemipteran-mediated transmission by subverting salicylic acid signaling pathway |
| title_sort | viral proteins resolve the virus vector conundrum during hemipteran mediated transmission by subverting salicylic acid signaling pathway |
| url | https://doi.org/10.1038/s41467-024-53894-y |
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