Viral proteins suppress rice defenses by boosting OsTSN1 RNA decay via phase separation and multimerization

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.

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Publication Details

Journal
Nature Communications
Published
2025-08-12
DOI
https://doi.org/10.1038/s41467-025-62395-5
Citations
6
Primary Topic
Plant Virus Research Studies
Type
article
Field-Weighted Citation Impact
10.50

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article

Viral proteins suppress rice defenses by boosting OsTSN1 RNA decay via phase separation and multimerization

Shibo Gao, Shuai Fu, Shifang Fei, Yunge Zhang et al.
6 citations
Nature Communications
Plant Virus Research Studies
10.50
article

Viral proteins suppress rice defenses by boosting OsTSN1 RNA decay via phase separation and multimerization

Shibo Gao, Shuai Fu, Shifang Fei, Yunge Zhang, Xueping Zhou, Tong Zhang, Dan Wang, Ming Zeng, Xuan Ye, Yaqin Wang, Lele Chen, You‐Ping Xu, Jianxiang Wu, Lianshun Zheng, Cui Zhang, Liyan Li
article en
6 citations

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.

Nature CommunicationsVol. 16(1)
South China Agricultural University (CN), Institute of Plant Protection (CN), Zhejiang Lab (CN), Chinese Academy of Agricultural Sciences (CN), Sanya University (CN), Center for Life Sciences (CN), Zhejiang University (CN)
Jiangsu Academy of Agricultural Sciences, National Natural Science Foundation of China, China Agricultural University, Zhejiang University, Earmarked Fund for Modern Agro-industry Technology Research System, National Key Research and Development Program of China
Zero hunger
Openalex Percentile: Top 2%
Plant Virus Research Studies
10.50
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