XCP1 cleaves Pathogenesis-related protein 1 into CAPE9 for systemic immunity in Arabidopsis
Abstract Proteolytic activation of cytokines regulates immunity in diverse organisms. In animals, cysteine-dependent aspartate-specific proteases (caspases) play central roles in cytokine maturation. Although the proteolytic production of peptide cytokines is also essential for plant immunity, evide...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2023-08-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-023-40406-7 |
| _version_ | 1797557804110708736 |
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| author | Ying-Lan Chen Fan-Wei Lin Kai-Tan Cheng Chi-Hsin Chang Sheng-Chi Hung Thomas Efferth Yet-Ran Chen |
| author_facet | Ying-Lan Chen Fan-Wei Lin Kai-Tan Cheng Chi-Hsin Chang Sheng-Chi Hung Thomas Efferth Yet-Ran Chen |
| author_sort | Ying-Lan Chen |
| collection | DOAJ |
| description | Abstract Proteolytic activation of cytokines regulates immunity in diverse organisms. In animals, cysteine-dependent aspartate-specific proteases (caspases) play central roles in cytokine maturation. Although the proteolytic production of peptide cytokines is also essential for plant immunity, evidence for cysteine-dependent aspartate-specific proteases in regulating plant immunity is still limited. In this study, we found that the C-terminal proteolytic processing of a caspase-like substrate motif “CNYD” within Pathogenesis-related protein 1 (PR1) generates an immunomodulatory cytokine (CAPE9) in Arabidopsis. Salicylic acid enhances CNYD-targeted protease activity and the proteolytic release of CAPE9 from PR1 in Arabidopsis. This process involves a protease exhibiting caspase-like enzyme activity, identified as Xylem cysteine peptidase 1 (XCP1). XCP1 exhibits a calcium-modulated pH-activity profile and a comparable activity to human caspases. XCP1 is required to induce systemic immunity triggered by pathogen-associated molecular patterns. This work reveals XCP1 as a key protease for plant immunity, which produces the cytokine CAPE9 from the canonical salicylic acid signaling marker PR1 to activate systemic immunity. |
| first_indexed | 2024-03-10T17:22:24Z |
| format | Article |
| id | doaj.art-5ae07089548c4bd6ae14ca845b9b26eb |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-10T17:22:24Z |
| publishDate | 2023-08-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-5ae07089548c4bd6ae14ca845b9b26eb2023-11-20T10:18:20ZengNature PortfolioNature Communications2041-17232023-08-0114111510.1038/s41467-023-40406-7XCP1 cleaves Pathogenesis-related protein 1 into CAPE9 for systemic immunity in ArabidopsisYing-Lan Chen0Fan-Wei Lin1Kai-Tan Cheng2Chi-Hsin Chang3Sheng-Chi Hung4Thomas Efferth5Yet-Ran Chen6Agricultural Biotechnology Research Center, Academia SinicaAgricultural Biotechnology Research Center, Academia SinicaAgricultural Biotechnology Research Center, Academia SinicaAgricultural Biotechnology Research Center, Academia SinicaAgricultural Biotechnology Research Center, Academia SinicaDepartment of Pharmaceutical Biology, Institute of Pharmaceutical and Biomedical Sciences, Johannes Gutenberg UniversityAgricultural Biotechnology Research Center, Academia SinicaAbstract Proteolytic activation of cytokines regulates immunity in diverse organisms. In animals, cysteine-dependent aspartate-specific proteases (caspases) play central roles in cytokine maturation. Although the proteolytic production of peptide cytokines is also essential for plant immunity, evidence for cysteine-dependent aspartate-specific proteases in regulating plant immunity is still limited. In this study, we found that the C-terminal proteolytic processing of a caspase-like substrate motif “CNYD” within Pathogenesis-related protein 1 (PR1) generates an immunomodulatory cytokine (CAPE9) in Arabidopsis. Salicylic acid enhances CNYD-targeted protease activity and the proteolytic release of CAPE9 from PR1 in Arabidopsis. This process involves a protease exhibiting caspase-like enzyme activity, identified as Xylem cysteine peptidase 1 (XCP1). XCP1 exhibits a calcium-modulated pH-activity profile and a comparable activity to human caspases. XCP1 is required to induce systemic immunity triggered by pathogen-associated molecular patterns. This work reveals XCP1 as a key protease for plant immunity, which produces the cytokine CAPE9 from the canonical salicylic acid signaling marker PR1 to activate systemic immunity.https://doi.org/10.1038/s41467-023-40406-7 |
| spellingShingle | Ying-Lan Chen Fan-Wei Lin Kai-Tan Cheng Chi-Hsin Chang Sheng-Chi Hung Thomas Efferth Yet-Ran Chen XCP1 cleaves Pathogenesis-related protein 1 into CAPE9 for systemic immunity in Arabidopsis Nature Communications |
| title | XCP1 cleaves Pathogenesis-related protein 1 into CAPE9 for systemic immunity in Arabidopsis |
| title_full | XCP1 cleaves Pathogenesis-related protein 1 into CAPE9 for systemic immunity in Arabidopsis |
| title_fullStr | XCP1 cleaves Pathogenesis-related protein 1 into CAPE9 for systemic immunity in Arabidopsis |
| title_full_unstemmed | XCP1 cleaves Pathogenesis-related protein 1 into CAPE9 for systemic immunity in Arabidopsis |
| title_short | XCP1 cleaves Pathogenesis-related protein 1 into CAPE9 for systemic immunity in Arabidopsis |
| title_sort | xcp1 cleaves pathogenesis related protein 1 into cape9 for systemic immunity in arabidopsis |
| url | https://doi.org/10.1038/s41467-023-40406-7 |
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