Reversible ubiquitination conferred by domain shuffling controls paired NLR immune receptor complex homeostasis in plant immunity
Abstract Plant intracellular NLR immune receptors can function individually or in pairs to detect pathogen effectors and activate immune responses. NLR homeostasis has to be tightly regulated to ensure proper defense without triggering autoimmunity. However, in contrast to singleton NLRs, the mechan...
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Nature Portfolio
2025-02-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-025-57231-9 |
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| author | Zhiyi Chen Jianhua Huang Jianyu Li Frank L. H. Menke Jonathan D. G. Jones Hailong Guo |
| author_facet | Zhiyi Chen Jianhua Huang Jianyu Li Frank L. H. Menke Jonathan D. G. Jones Hailong Guo |
| author_sort | Zhiyi Chen |
| collection | DOAJ |
| description | Abstract Plant intracellular NLR immune receptors can function individually or in pairs to detect pathogen effectors and activate immune responses. NLR homeostasis has to be tightly regulated to ensure proper defense without triggering autoimmunity. However, in contrast to singleton NLRs, the mechanisms controlling the paired NLRs complex homeostasis are less understood. The paired Arabidopsis RRS1/RPS4 immune receptor complex confers disease resistance through effector recognition mediated by the integrated WRKY domain of RRS1. Here, through proximity labeling, we reveal a ubiquitination-deubiquitination cycle that controls the homeostasis of the RRS1/RPS4 complex. E3 ligase RARE directly binds and ubiquitinates RRS1’s WRKY domain to promote its proteasomal degradation, thereby destabilizing RPS4 indirectly and compromising the stability and function of the RRS1/RPS4 complex. Conversely, the deubiquitinating enzymes UBP12/UBP13 deubiquitinate RRS1’s WRKY domain, counteracting RARE’s effects. Interestingly, the abundance of WRKY transcription factors WRKY70 and WRKY41 is also regulated by RARE and UBP12/UBP13. Phylogenetic analysis suggests this regulation likely transferred from WRKY70/WRKY41 to RRS1 upon WRKY domain integration. Our findings improve our understanding of homeostatic regulation of paired NLR complex and uncover a paradigm whereby domain integration can co-opt preexisting post-translational modification to regulate novel protein functions. |
| format | Article |
| id | doaj-art-a13881de255842e190d16be72cbbcce1 |
| institution | DOAJ |
| issn | 2041-1723 |
| language | English |
| publishDate | 2025-02-01 |
| publisher | Nature Portfolio |
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| spelling | doaj-art-a13881de255842e190d16be72cbbcce12025-08-20T03:04:02ZengNature PortfolioNature Communications2041-17232025-02-0116111510.1038/s41467-025-57231-9Reversible ubiquitination conferred by domain shuffling controls paired NLR immune receptor complex homeostasis in plant immunityZhiyi Chen0Jianhua Huang1Jianyu Li2Frank L. H. Menke3Jonathan D. G. Jones4Hailong Guo5State Key Laboratory of Agricultural and Forestry Biosecurity, Department of Plant Pathology, China Agricultural UniversityThe Sainsbury Laboratory, University of East Anglia, Norwich Research ParkState Key Laboratory of Agricultural and Forestry Biosecurity, Department of Plant Pathology, China Agricultural UniversityThe Sainsbury Laboratory, University of East Anglia, Norwich Research ParkThe Sainsbury Laboratory, University of East Anglia, Norwich Research ParkState Key Laboratory of Agricultural and Forestry Biosecurity, Department of Plant Pathology, China Agricultural UniversityAbstract Plant intracellular NLR immune receptors can function individually or in pairs to detect pathogen effectors and activate immune responses. NLR homeostasis has to be tightly regulated to ensure proper defense without triggering autoimmunity. However, in contrast to singleton NLRs, the mechanisms controlling the paired NLRs complex homeostasis are less understood. The paired Arabidopsis RRS1/RPS4 immune receptor complex confers disease resistance through effector recognition mediated by the integrated WRKY domain of RRS1. Here, through proximity labeling, we reveal a ubiquitination-deubiquitination cycle that controls the homeostasis of the RRS1/RPS4 complex. E3 ligase RARE directly binds and ubiquitinates RRS1’s WRKY domain to promote its proteasomal degradation, thereby destabilizing RPS4 indirectly and compromising the stability and function of the RRS1/RPS4 complex. Conversely, the deubiquitinating enzymes UBP12/UBP13 deubiquitinate RRS1’s WRKY domain, counteracting RARE’s effects. Interestingly, the abundance of WRKY transcription factors WRKY70 and WRKY41 is also regulated by RARE and UBP12/UBP13. Phylogenetic analysis suggests this regulation likely transferred from WRKY70/WRKY41 to RRS1 upon WRKY domain integration. Our findings improve our understanding of homeostatic regulation of paired NLR complex and uncover a paradigm whereby domain integration can co-opt preexisting post-translational modification to regulate novel protein functions.https://doi.org/10.1038/s41467-025-57231-9 |
| spellingShingle | Zhiyi Chen Jianhua Huang Jianyu Li Frank L. H. Menke Jonathan D. G. Jones Hailong Guo Reversible ubiquitination conferred by domain shuffling controls paired NLR immune receptor complex homeostasis in plant immunity Nature Communications |
| title | Reversible ubiquitination conferred by domain shuffling controls paired NLR immune receptor complex homeostasis in plant immunity |
| title_full | Reversible ubiquitination conferred by domain shuffling controls paired NLR immune receptor complex homeostasis in plant immunity |
| title_fullStr | Reversible ubiquitination conferred by domain shuffling controls paired NLR immune receptor complex homeostasis in plant immunity |
| title_full_unstemmed | Reversible ubiquitination conferred by domain shuffling controls paired NLR immune receptor complex homeostasis in plant immunity |
| title_short | Reversible ubiquitination conferred by domain shuffling controls paired NLR immune receptor complex homeostasis in plant immunity |
| title_sort | reversible ubiquitination conferred by domain shuffling controls paired nlr immune receptor complex homeostasis in plant immunity |
| url | https://doi.org/10.1038/s41467-025-57231-9 |
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