Exportin-4 coordinates nuclear shuttling of TOPLESS family transcription corepressors to regulate plant immunity
The regulated nucleocytoplasmic exchange of macromolecules is essential for the eukaryotic cell. However, nuclear transport pathways defined by different nuclear transport receptors (NTRs), including importins and exportins, and their significance in activating distinct stress responses are poorly u...
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| Published in | The Plant cell Vol. 33; no. 3; pp. 697 - 713 |
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| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
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05.05.2021
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| Abstract | The regulated nucleocytoplasmic exchange of macromolecules is essential for the eukaryotic cell. However, nuclear transport pathways defined by different nuclear transport receptors (NTRs), including importins and exportins, and their significance in activating distinct stress responses are poorly understood in plants. Here, we exploited a CRISPR/Cas9-based genetic screen to search for modifiers of CONSTITUTIVE EXPRESSION OF PATHOGENESIS-RELATED GENE 5 (cpr5), an Arabidopsis thaliana nucleoporin mutant that activates autoimmune responses that partially mimic effector-triggered immunity (ETI). We identified an NTR gene, Exportin-4 (XPO4), as a genetic interactor of CPR5. The xpo4 cpr5 double mutant activates catastrophic immune responses, which leads to seedling lethality. By leveraging the newly developed proximity-labeling proteomics, we profiled XPO4 substrates and identified TOPLESS (TPL) and TPL-related (TPR) transcription corepressors as XPO4-specific cargo. TPL/TPRs target negative regulators of immunity and are redundantly required for ETI induction. We found that loss-of-XPO4 promotes the nuclear accumulation of TPL/TPRs in the presence of elevated salicylic acid (SA), which contributes to the SA-mediated defense amplification and potentiates immune induction in the cpr5 mutant. We showed that TPL and TPRs are required for the enhanced immune activation observed in xpo4 cpr5 but not for the cpr5 single-mutant phenotype, underscoring the functional interplay between XPO4 and TPL/TPRs and its importance in cpr5-dependent immune induction. We propose that XPO4 coordinates the nuclear accumulation of TPL/TPRs, which plays a role in regulating SA-mediated defense feedback to modulate immune strength downstream of CPR5 during ETI induction. |
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| AbstractList | Abstract
The regulated nucleocytoplasmic exchange of macromolecules is essential for the eukaryotic cell. However, nuclear transport pathways defined by different nuclear transport receptors (NTRs), including importins and exportins, and their significance in activating distinct stress responses are poorly understood in plants. Here, we exploited a CRISPR/Cas9-based genetic screen to search for modifiers of CONSTITUTIVE EXPRESSION OF PATHOGENESIS-RELATED GENE 5 (cpr5), an Arabidopsis thaliana nucleoporin mutant that activates autoimmune responses that partially mimic effector-triggered immunity (ETI). We identified an NTR gene, Exportin-4 (XPO4), as a genetic interactor of CPR5. The xpo4 cpr5 double mutant activates catastrophic immune responses, which leads to seedling lethality. By leveraging the newly developed proximity-labeling proteomics, we profiled XPO4 substrates and identified TOPLESS (TPL) and TPL-related (TPR) transcription corepressors as XPO4-specific cargo. TPL/TPRs target negative regulators of immunity and are redundantly required for ETI induction. We found that loss-of-XPO4 promotes the nuclear accumulation of TPL/TPRs in the presence of elevated salicylic acid (SA), which contributes to the SA-mediated defense amplification and potentiates immune induction in the cpr5 mutant. We showed that TPL and TPRs are required for the enhanced immune activation observed in xpo4 cpr5 but not for the cpr5 single-mutant phenotype, underscoring the functional interplay between XPO4 and TPL/TPRs and its importance in cpr5-dependent immune induction. We propose that XPO4 coordinates the nuclear accumulation of TPL/TPRs, which plays a role in regulating SA-mediated defense feedback to modulate immune strength downstream of CPR5 during ETI induction. The regulated nucleocytoplasmic exchange of macromolecules is essential for the eukaryotic cell. However, nuclear transport pathways defined by different nuclear transport receptors (NTRs), including importins and exportins, and their significance in activating distinct stress responses are poorly understood in plants. Here, we exploited a CRISPR/Cas9-based genetic screen to search for modifiers of CONSTITUTIVE EXPRESSION OF PATHOGENESIS-RELATED GENE 5 (cpr5), an Arabidopsis thaliana nucleoporin mutant that activates autoimmune responses that partially mimic effector-triggered immunity (ETI). We identified an NTR gene, Exportin-4 (XPO4), as a genetic interactor of CPR5. The xpo4 cpr5 double mutant activates catastrophic immune responses, which leads to seedling lethality. By leveraging the newly developed proximity-labeling proteomics, we profiled XPO4 substrates and identified TOPLESS (TPL) and TPL-related (TPR) transcription corepressors as XPO4-specific cargo. TPL/TPRs target negative regulators of immunity and are redundantly required for ETI induction. We found that loss-of-XPO4 promotes the nuclear accumulation of TPL/TPRs in the presence of elevated salicylic acid (SA), which contributes to the SA-mediated defense amplification and potentiates immune induction in the cpr5 mutant. We showed that TPL and TPRs are required for the enhanced immune activation observed in xpo4 cpr5 but not for the cpr5 single-mutant phenotype, underscoring the functional interplay between XPO4 and TPL/TPRs and its importance in cpr5-dependent immune induction. We propose that XPO4 coordinates the nuclear accumulation of TPL/TPRs, which plays a role in regulating SA-mediated defense feedback to modulate immune strength downstream of CPR5 during ETI induction. |
| Author | Tang, Yu Bao, Jinsong Xu, Feifei Jia, Min Jiang, Keni Li, Xin Gu, Yangnan |
| Author_xml | – sequence: 1 givenname: Feifei surname: Xu fullname: Xu, Feifei organization: Institute of Nuclear Agricultural Sciences, Key Laboratory for Nuclear Agricultural Sciences of Zhejiang Province and Ministry of Agriculture and Rural Affairs, Zhejiang University, Zijingang Campus, Hangzhou 310058, China – sequence: 2 givenname: Min surname: Jia fullname: Jia, Min organization: Innovative Genomics Institute, University of California, Berkeley, California 94720, USA – sequence: 3 givenname: Xin surname: Li fullname: Li, Xin organization: Innovative Genomics Institute, University of California, Berkeley, California 94720, USA – sequence: 4 givenname: Yu surname: Tang fullname: Tang, Yu organization: Innovative Genomics Institute, University of California, Berkeley, California 94720, USA – sequence: 5 givenname: Keni surname: Jiang fullname: Jiang, Keni organization: Department of Plant and Microbial Biology, University of California, Berkeley, California 94720, USA – sequence: 6 givenname: Jinsong surname: Bao fullname: Bao, Jinsong organization: Institute of Nuclear Agricultural Sciences, Key Laboratory for Nuclear Agricultural Sciences of Zhejiang Province and Ministry of Agriculture and Rural Affairs, Zhejiang University, Zijingang Campus, Hangzhou 310058, China – sequence: 7 givenname: Yangnan surname: Gu fullname: Gu, Yangnan organization: Innovative Genomics Institute, University of California, Berkeley, California 94720, USA |
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