A Phase‐Separated SR Protein Reprograms Host Pre‐mRNA Splicing to Enhance Disease Susceptibility
Abstract Alternative splicing (AS) plays a vital role in the plant–microbe interaction. Modulating host precursor‐mRNA AS is a key strategy employed by multiple pathogens to subvert plant immunity. However, the underlying mechanism by which the host splicing factor regulates plant immunity remains p...
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Wiley
2025-07-01
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| Series: | Advanced Science |
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| Online Access: | https://doi.org/10.1002/advs.202500072 |
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| author | Dong Yan Jie Huang Fengqi Tian Haidong Shu Han Chen Qian Peng Hongwei Wu Jianlong Zhao Anireddy S. N. Reddy Gang Li Yuanchao Wang Suomeng Dong |
| author_facet | Dong Yan Jie Huang Fengqi Tian Haidong Shu Han Chen Qian Peng Hongwei Wu Jianlong Zhao Anireddy S. N. Reddy Gang Li Yuanchao Wang Suomeng Dong |
| author_sort | Dong Yan |
| collection | DOAJ |
| description | Abstract Alternative splicing (AS) plays a vital role in the plant–microbe interaction. Modulating host precursor‐mRNA AS is a key strategy employed by multiple pathogens to subvert plant immunity. However, the underlying mechanism by which the host splicing factor regulates plant immunity remains poorly understood. Here, a plant‐conserved serine/arginine‐rich (SR) RNA splicing factor, SR30, which negatively regulates tomato immunity against the infamous Phytophthora infestans (P. infestans) is identified. SR30 governs tomato mRNA AS at a genome‐wide level and suppresses defense‐related genes AS. During P. infestans infection, SR30 is induced to form nuclear condensates via liquid–liquid phase separation driven by intrinsically disordered regions. Importantly, the phase separation property is required for the function of SR30 in disease susceptibility and the regulation of genes AS. Knockout of SR30 via CRISPR/Cas9 improves tomato disease resistance to P. infestans, P. capsici, and P. parasitica by promoting defense genes AS. These findings uncover a novel mechanism in a phase‐separated protein that regulates plant immunity by altering the AS of defense‐related genes and provides a new paradigm for engineering protein condensate in crop‐resistant breeding. |
| format | Article |
| id | doaj-art-bff072534db543e6ad9fabc423e83a7e |
| institution | DOAJ |
| issn | 2198-3844 |
| language | English |
| publishDate | 2025-07-01 |
| publisher | Wiley |
| record_format | Article |
| series | Advanced Science |
| spelling | doaj-art-bff072534db543e6ad9fabc423e83a7e2025-08-20T03:12:04ZengWileyAdvanced Science2198-38442025-07-011227n/an/a10.1002/advs.202500072A Phase‐Separated SR Protein Reprograms Host Pre‐mRNA Splicing to Enhance Disease SusceptibilityDong Yan0Jie Huang1Fengqi Tian2Haidong Shu3Han Chen4Qian Peng5Hongwei Wu6Jianlong Zhao7Anireddy S. N. Reddy8Gang Li9Yuanchao Wang10Suomeng Dong11State Key Laboratory of Agricultural and Forestry Biosecurity College of Plant Protection Nanjing Agricultural University Nanjing 210095 ChinaThe Plant Chemetics Laboratory Department of Biology University of Oxford Oxford OX1 3RB UKState Key Laboratory of Agricultural and Forestry Biosecurity College of Plant Protection Nanjing Agricultural University Nanjing 210095 ChinaState Key Laboratory of Agricultural and Forestry Biosecurity College of Plant Protection Nanjing Agricultural University Nanjing 210095 ChinaState Key Laboratory of Agricultural and Forestry Biosecurity College of Plant Protection Nanjing Agricultural University Nanjing 210095 ChinaState Key Laboratory of Agricultural and Forestry Biosecurity College of Plant Protection Nanjing Agricultural University Nanjing 210095 ChinaState Key Laboratory of Agricultural and Forestry Biosecurity College of Plant Protection Nanjing Agricultural University Nanjing 210095 ChinaState Key Laboratory of Vegetable Biobreeding Institute of Vegetables and Flowers Chinese Academy of Agricultural Sciences Beijing 100081 ChinaDepartment of Biology and Program in Cell and Molecular Biology Colorado State University Fort Collins CO 80523 USAState Key Laboratory of Agricultural and Forestry Biosecurity College of Plant Protection Nanjing Agricultural University Nanjing 210095 ChinaState Key Laboratory of Agricultural and Forestry Biosecurity College of Plant Protection Nanjing Agricultural University Nanjing 210095 ChinaState Key Laboratory of Agricultural and Forestry Biosecurity College of Plant Protection Nanjing Agricultural University Nanjing 210095 ChinaAbstract Alternative splicing (AS) plays a vital role in the plant–microbe interaction. Modulating host precursor‐mRNA AS is a key strategy employed by multiple pathogens to subvert plant immunity. However, the underlying mechanism by which the host splicing factor regulates plant immunity remains poorly understood. Here, a plant‐conserved serine/arginine‐rich (SR) RNA splicing factor, SR30, which negatively regulates tomato immunity against the infamous Phytophthora infestans (P. infestans) is identified. SR30 governs tomato mRNA AS at a genome‐wide level and suppresses defense‐related genes AS. During P. infestans infection, SR30 is induced to form nuclear condensates via liquid–liquid phase separation driven by intrinsically disordered regions. Importantly, the phase separation property is required for the function of SR30 in disease susceptibility and the regulation of genes AS. Knockout of SR30 via CRISPR/Cas9 improves tomato disease resistance to P. infestans, P. capsici, and P. parasitica by promoting defense genes AS. These findings uncover a novel mechanism in a phase‐separated protein that regulates plant immunity by altering the AS of defense‐related genes and provides a new paradigm for engineering protein condensate in crop‐resistant breeding.https://doi.org/10.1002/advs.202500072alternative splicinglate blight diseasephase separationplant immunitySR proteins |
| spellingShingle | Dong Yan Jie Huang Fengqi Tian Haidong Shu Han Chen Qian Peng Hongwei Wu Jianlong Zhao Anireddy S. N. Reddy Gang Li Yuanchao Wang Suomeng Dong A Phase‐Separated SR Protein Reprograms Host Pre‐mRNA Splicing to Enhance Disease Susceptibility Advanced Science alternative splicing late blight disease phase separation plant immunity SR proteins |
| title | A Phase‐Separated SR Protein Reprograms Host Pre‐mRNA Splicing to Enhance Disease Susceptibility |
| title_full | A Phase‐Separated SR Protein Reprograms Host Pre‐mRNA Splicing to Enhance Disease Susceptibility |
| title_fullStr | A Phase‐Separated SR Protein Reprograms Host Pre‐mRNA Splicing to Enhance Disease Susceptibility |
| title_full_unstemmed | A Phase‐Separated SR Protein Reprograms Host Pre‐mRNA Splicing to Enhance Disease Susceptibility |
| title_short | A Phase‐Separated SR Protein Reprograms Host Pre‐mRNA Splicing to Enhance Disease Susceptibility |
| title_sort | phase separated sr protein reprograms host pre mrna splicing to enhance disease susceptibility |
| topic | alternative splicing late blight disease phase separation plant immunity SR proteins |
| url | https://doi.org/10.1002/advs.202500072 |
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