Commensal lifestyle regulated by a negative feedback loop between Arabidopsis ROS and the bacterial T2SS
Abstract Despite the plant health-promoting effects of plant microbiota, these assemblages also comprise potentially detrimental microbes. How plant immunity controls its microbiota to promote plant health under these conditions remains largely unknown. We find that commensal bacteria isolated from...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-01-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-44724-2 |
| _version_ | 1797355680160546816 |
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| author | Frederickson Entila Xiaowei Han Akira Mine Paul Schulze-Lefert Kenichi Tsuda |
| author_facet | Frederickson Entila Xiaowei Han Akira Mine Paul Schulze-Lefert Kenichi Tsuda |
| author_sort | Frederickson Entila |
| collection | DOAJ |
| description | Abstract Despite the plant health-promoting effects of plant microbiota, these assemblages also comprise potentially detrimental microbes. How plant immunity controls its microbiota to promote plant health under these conditions remains largely unknown. We find that commensal bacteria isolated from healthy Arabidopsis plants trigger diverse patterns of reactive oxygen species (ROS) production dependent on the immune receptors and completely on the NADPH oxidase RBOHD that selectively inhibited specific commensals, notably Xanthomonas L148. Through random mutagenesis, we find that L148 gspE, encoding a type II secretion system (T2SS) component, is required for the damaging effects of Xanthomonas L148 on rbohD mutant plants. In planta bacterial transcriptomics reveals that RBOHD suppresses most T2SS gene expression including gspE. L148 colonization protected plants against a bacterial pathogen, when gspE was inhibited by ROS or mutation. Thus, a negative feedback loop between Arabidopsis ROS and the bacterial T2SS tames a potentially detrimental leaf commensal and turns it into a microbe beneficial to the host. |
| first_indexed | 2024-03-08T14:14:36Z |
| format | Article |
| id | doaj.art-df6d1264cdb74eb9adc21abb6c37fba5 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-03-08T14:14:36Z |
| publishDate | 2024-01-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-df6d1264cdb74eb9adc21abb6c37fba52024-01-14T12:29:42ZengNature PortfolioNature Communications2041-17232024-01-0115111710.1038/s41467-024-44724-2Commensal lifestyle regulated by a negative feedback loop between Arabidopsis ROS and the bacterial T2SSFrederickson Entila0Xiaowei Han1Akira Mine2Paul Schulze-Lefert3Kenichi Tsuda4National Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Hubei Key Laboratory of Plant Pathology, College of Plant Science and Technology, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Hubei Key Laboratory of Plant Pathology, College of Plant Science and Technology, Huazhong Agricultural UniversityJST PRESTODepartment of Plant Microbe Interactions, Max Planck Institute for Plant Breeding ResearchNational Key Laboratory of Agricultural Microbiology, Hubei Hongshan Laboratory, Hubei Key Laboratory of Plant Pathology, College of Plant Science and Technology, Huazhong Agricultural UniversityAbstract Despite the plant health-promoting effects of plant microbiota, these assemblages also comprise potentially detrimental microbes. How plant immunity controls its microbiota to promote plant health under these conditions remains largely unknown. We find that commensal bacteria isolated from healthy Arabidopsis plants trigger diverse patterns of reactive oxygen species (ROS) production dependent on the immune receptors and completely on the NADPH oxidase RBOHD that selectively inhibited specific commensals, notably Xanthomonas L148. Through random mutagenesis, we find that L148 gspE, encoding a type II secretion system (T2SS) component, is required for the damaging effects of Xanthomonas L148 on rbohD mutant plants. In planta bacterial transcriptomics reveals that RBOHD suppresses most T2SS gene expression including gspE. L148 colonization protected plants against a bacterial pathogen, when gspE was inhibited by ROS or mutation. Thus, a negative feedback loop between Arabidopsis ROS and the bacterial T2SS tames a potentially detrimental leaf commensal and turns it into a microbe beneficial to the host.https://doi.org/10.1038/s41467-024-44724-2 |
| spellingShingle | Frederickson Entila Xiaowei Han Akira Mine Paul Schulze-Lefert Kenichi Tsuda Commensal lifestyle regulated by a negative feedback loop between Arabidopsis ROS and the bacterial T2SS Nature Communications |
| title | Commensal lifestyle regulated by a negative feedback loop between Arabidopsis ROS and the bacterial T2SS |
| title_full | Commensal lifestyle regulated by a negative feedback loop between Arabidopsis ROS and the bacterial T2SS |
| title_fullStr | Commensal lifestyle regulated by a negative feedback loop between Arabidopsis ROS and the bacterial T2SS |
| title_full_unstemmed | Commensal lifestyle regulated by a negative feedback loop between Arabidopsis ROS and the bacterial T2SS |
| title_short | Commensal lifestyle regulated by a negative feedback loop between Arabidopsis ROS and the bacterial T2SS |
| title_sort | commensal lifestyle regulated by a negative feedback loop between arabidopsis ros and the bacterial t2ss |
| url | https://doi.org/10.1038/s41467-024-44724-2 |
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