Viral proteins suppress rice defenses by boosting OsTSN1 RNA decay via phase separation and multimerization
Abstract Liquid-liquid phase separation (LLPS) forms membraneless condensates crucial for plant stress responses. However, how plant viruses utilize LLPS to escape host immunity remains largely unexplored. Here, we show that P6 protein encoded by southern rice black-streaked dwarf virus (SRBSDV) und...
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Nature Portfolio
2025-08-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-025-62395-5 |
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| author | Ming Zeng Shuai Fu Youping Xu Liyan Li Dan Wang Shi-bo Gao Lianshun Zheng Yunge Zhang Cui Zhang Shifang Fei Xuan Ye Lele Chen Yaqin Wang Tong Zhang Xueping Zhou Jianxiang Wu |
| author_facet | Ming Zeng Shuai Fu Youping Xu Liyan Li Dan Wang Shi-bo Gao Lianshun Zheng Yunge Zhang Cui Zhang Shifang Fei Xuan Ye Lele Chen Yaqin Wang Tong Zhang Xueping Zhou Jianxiang Wu |
| author_sort | Ming Zeng |
| collection | DOAJ |
| description | Abstract Liquid-liquid phase separation (LLPS) forms membraneless condensates crucial for plant stress responses. However, how plant viruses utilize LLPS to escape host immunity remains largely unexplored. Here, we show that P6 protein encoded by southern rice black-streaked dwarf virus (SRBSDV) undergoes LLPS. P6 interacts with OsTSN1 to form the P6-OsTSN1-containing droplets co-localized with stress granules (SGs). Within these droplets, P6 enhances OsTSN1 nuclease activity via promoting its multimerization to degrade transcripts with G-A-rich motifs of two transcription factors (TFs), OsNAC15 and OsLHY. These two TFs regulate the transcription of OsJAZ6, OsJAZ12, and OsATG8C, key components of jasmonic acid (JA)- and autophagy-associated defense pathways. Furthermore, the degradation of OsNAC15 and OsLHY transcripts in P6-OsTSN1-containing droplets weakens JA- and autophagy-mediated defenses in rice, facilitating SRBSDV infection. Additionally, similar to SRBSDV P6, intrinsically disordered region (IDR)-containing RNA silencing suppressors encoded by rice black-streaked dwarf virus and rice stripe virus, also interact with OsTSN1, promoting the degradation of OsNAC15 and OsLHY transcripts to enhance viral infection. Our findings indicate that OsTSN1 acts as a central positive regulator of virus infection in rice, convergently co-opted by viruses. These insights help us to better understand the roles of LLPS and OsTSN1 in virus infection in rice. |
| format | Article |
| id | doaj-art-0fc75a8451cc49adab492bfbb90febf3 |
| institution | DOAJ |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-08-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj-art-0fc75a8451cc49adab492bfbb90febf32025-08-20T03:05:06ZengNature PortfolioNature Communications2041-17232025-08-0116112410.1038/s41467-025-62395-5Viral proteins suppress rice defenses by boosting OsTSN1 RNA decay via phase separation and multimerizationMing Zeng0Shuai Fu1Youping Xu2Liyan Li3Dan Wang4Shi-bo Gao5Lianshun Zheng6Yunge Zhang7Cui Zhang8Shifang Fei9Xuan Ye10Lele Chen11Yaqin Wang12Tong Zhang13Xueping Zhou14Jianxiang Wu15State Key Laboratory of Rice Biology and Breeding, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang UniversityState Key Laboratory of Rice Biology and Breeding, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang UniversityAnalysis Center of Agrobiology and Environmental Sciences, Zhejiang UniversityState Key Laboratory of Rice Biology and Breeding, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang UniversityState Key Laboratory of Rice Biology and Breeding, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang UniversityState Key Laboratory of Rice Biology and Breeding, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang UniversityState Key Laboratory of Rice Biology and Breeding, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang UniversityState Key Laboratory of Rice Biology and Breeding, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang UniversityState Key Laboratory of Rice Biology and Breeding, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang UniversityState Key Laboratory of Rice Biology and Breeding, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang UniversityState Key Laboratory of Rice Biology and Breeding, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang UniversityState Key Laboratory of Rice Biology and Breeding, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang UniversityState Key Laboratory of Rice Biology and Breeding, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang UniversityGuangdong Province Key Laboratory of Microbial Signals and Disease Control, College of Plant Protection, South China Agricultural UniversityState Key Laboratory of Rice Biology and Breeding, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang UniversityState Key Laboratory of Rice Biology and Breeding, Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Biotechnology, Zhejiang UniversityAbstract Liquid-liquid phase separation (LLPS) forms membraneless condensates crucial for plant stress responses. However, how plant viruses utilize LLPS to escape host immunity remains largely unexplored. Here, we show that P6 protein encoded by southern rice black-streaked dwarf virus (SRBSDV) undergoes LLPS. P6 interacts with OsTSN1 to form the P6-OsTSN1-containing droplets co-localized with stress granules (SGs). Within these droplets, P6 enhances OsTSN1 nuclease activity via promoting its multimerization to degrade transcripts with G-A-rich motifs of two transcription factors (TFs), OsNAC15 and OsLHY. These two TFs regulate the transcription of OsJAZ6, OsJAZ12, and OsATG8C, key components of jasmonic acid (JA)- and autophagy-associated defense pathways. Furthermore, the degradation of OsNAC15 and OsLHY transcripts in P6-OsTSN1-containing droplets weakens JA- and autophagy-mediated defenses in rice, facilitating SRBSDV infection. Additionally, similar to SRBSDV P6, intrinsically disordered region (IDR)-containing RNA silencing suppressors encoded by rice black-streaked dwarf virus and rice stripe virus, also interact with OsTSN1, promoting the degradation of OsNAC15 and OsLHY transcripts to enhance viral infection. Our findings indicate that OsTSN1 acts as a central positive regulator of virus infection in rice, convergently co-opted by viruses. These insights help us to better understand the roles of LLPS and OsTSN1 in virus infection in rice.https://doi.org/10.1038/s41467-025-62395-5 |
| spellingShingle | Ming Zeng Shuai Fu Youping Xu Liyan Li Dan Wang Shi-bo Gao Lianshun Zheng Yunge Zhang Cui Zhang Shifang Fei Xuan Ye Lele Chen Yaqin Wang Tong Zhang Xueping Zhou Jianxiang Wu Viral proteins suppress rice defenses by boosting OsTSN1 RNA decay via phase separation and multimerization Nature Communications |
| title | Viral proteins suppress rice defenses by boosting OsTSN1 RNA decay via phase separation and multimerization |
| title_full | Viral proteins suppress rice defenses by boosting OsTSN1 RNA decay via phase separation and multimerization |
| title_fullStr | Viral proteins suppress rice defenses by boosting OsTSN1 RNA decay via phase separation and multimerization |
| title_full_unstemmed | Viral proteins suppress rice defenses by boosting OsTSN1 RNA decay via phase separation and multimerization |
| title_short | Viral proteins suppress rice defenses by boosting OsTSN1 RNA decay via phase separation and multimerization |
| title_sort | viral proteins suppress rice defenses by boosting ostsn1 rna decay via phase separation and multimerization |
| url | https://doi.org/10.1038/s41467-025-62395-5 |
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