A new type III effector from Bradyrhizobium sp. DOA9 encoding a putative SUMO-protease blocks nodulation in Arachis hypogaea L.
Abstract Effector proteins secreted via the type III secretion system (T3SS) of nitrogen-fixing rhizobia are key determinants of symbiotic compatibility in legumes. Previous report revealed that the T3SS of Bradyrhizobium sp. DOA9 plays negative effects on Arachis hypogaea symbiosis. In this study,...
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Nature Portfolio
2024-12-01
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| Series: | Scientific Reports |
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| Online Access: | https://doi.org/10.1038/s41598-024-78913-2 |
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| author | Beedou Aphaiso Pongdet Piromyou Pakpoom Boonchuen Pongpan Songwattana Jenjira Wongdee Teerana Greetatorn Kamonluck Teamtisong Alicia Camuel Panlada Tittabutr Nantakorn Boonkerd Eric Giraud Neung Teaumroong |
| author_facet | Beedou Aphaiso Pongdet Piromyou Pakpoom Boonchuen Pongpan Songwattana Jenjira Wongdee Teerana Greetatorn Kamonluck Teamtisong Alicia Camuel Panlada Tittabutr Nantakorn Boonkerd Eric Giraud Neung Teaumroong |
| author_sort | Beedou Aphaiso |
| collection | DOAJ |
| description | Abstract Effector proteins secreted via the type III secretion system (T3SS) of nitrogen-fixing rhizobia are key determinants of symbiotic compatibility in legumes. Previous report revealed that the T3SS of Bradyrhizobium sp. DOA9 plays negative effects on Arachis hypogaea symbiosis. In this study, we characterized the symbiotic role of 4 effector proteins (p0490, p0871, SkP48, and p0903) containing the small ubiquitin-like modifier (SUMO) protease domain identified in DOA9 during symbiosis. While the DOA9 strain and the two mutants of SUMO-proteases, p0490 and p0871, induced inefficient nodulation in A. hypogaea, the mutation of SUMO-proteases SkP48 or p0903 promoted efficient symbiosis comparable to the type strain Bradyrhizobium arachidis CCBAU051107. Complementation study of ∆p0903 with various mutated forms of p0903 highlighted importance of ubiquitin-like protein (ULP) domain in restriction of nodulation in A. hypogaea. We observed the accumulation of jasmonic acid (JA) and upregulation of several defence genes involved in the JA/ethylene (ET) signalling pathway at the early stage of infection in roots inoculated with DOA9 strain compared with those inoculated with the DOA9-∆p0903 strain. Our data highlight the importance of SUMO-protease effectors during the symbiotic interaction between bradyrhizobia and A. hypogaea, which could be useful for the development of high-performance inocula to improve its growth. |
| format | Article |
| id | doaj-art-f5a91a549ce940f687e5daaa64c6e9ea |
| institution | Kabale University |
| issn | 2045-2322 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | Nature Portfolio |
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| series | Scientific Reports |
| spelling | doaj-art-f5a91a549ce940f687e5daaa64c6e9ea2025-01-05T12:27:10ZengNature PortfolioScientific Reports2045-23222024-12-0114111510.1038/s41598-024-78913-2A new type III effector from Bradyrhizobium sp. DOA9 encoding a putative SUMO-protease blocks nodulation in Arachis hypogaea L.Beedou Aphaiso0Pongdet Piromyou1Pakpoom Boonchuen2Pongpan Songwattana3Jenjira Wongdee4Teerana Greetatorn5Kamonluck Teamtisong6Alicia Camuel7Panlada Tittabutr8Nantakorn Boonkerd9Eric Giraud10Neung Teaumroong11School of Biotechnology, Institute of Agricultural Technology, Suranaree University of TechnologyInstitute of Research and Development, Suranaree University of TechnologySchool of Biotechnology, Institute of Agricultural Technology, Suranaree University of TechnologyInstitute of Research and Development, Suranaree University of TechnologyInstitute of Research and Development, Suranaree University of TechnologyInstitute of Research and Development, Suranaree University of TechnologyThe Center for Scientific and Technological Equipment, Suranaree University of TechnologyIRD/CIRAD/INRAE, PHIM, Plant Health Institute of Montpellier, UMR-PHIM, Université de Montpellier/Institut AgroSchool of Biotechnology, Institute of Agricultural Technology, Suranaree University of TechnologySchool of Biotechnology, Institute of Agricultural Technology, Suranaree University of TechnologyIRD/CIRAD/INRAE, PHIM, Plant Health Institute of Montpellier, UMR-PHIM, Université de Montpellier/Institut AgroSchool of Biotechnology, Institute of Agricultural Technology, Suranaree University of TechnologyAbstract Effector proteins secreted via the type III secretion system (T3SS) of nitrogen-fixing rhizobia are key determinants of symbiotic compatibility in legumes. Previous report revealed that the T3SS of Bradyrhizobium sp. DOA9 plays negative effects on Arachis hypogaea symbiosis. In this study, we characterized the symbiotic role of 4 effector proteins (p0490, p0871, SkP48, and p0903) containing the small ubiquitin-like modifier (SUMO) protease domain identified in DOA9 during symbiosis. While the DOA9 strain and the two mutants of SUMO-proteases, p0490 and p0871, induced inefficient nodulation in A. hypogaea, the mutation of SUMO-proteases SkP48 or p0903 promoted efficient symbiosis comparable to the type strain Bradyrhizobium arachidis CCBAU051107. Complementation study of ∆p0903 with various mutated forms of p0903 highlighted importance of ubiquitin-like protein (ULP) domain in restriction of nodulation in A. hypogaea. We observed the accumulation of jasmonic acid (JA) and upregulation of several defence genes involved in the JA/ethylene (ET) signalling pathway at the early stage of infection in roots inoculated with DOA9 strain compared with those inoculated with the DOA9-∆p0903 strain. Our data highlight the importance of SUMO-protease effectors during the symbiotic interaction between bradyrhizobia and A. hypogaea, which could be useful for the development of high-performance inocula to improve its growth.https://doi.org/10.1038/s41598-024-78913-2Bradyrhizobium spArachis hypogaeaT3SSand SUMO-protease |
| spellingShingle | Beedou Aphaiso Pongdet Piromyou Pakpoom Boonchuen Pongpan Songwattana Jenjira Wongdee Teerana Greetatorn Kamonluck Teamtisong Alicia Camuel Panlada Tittabutr Nantakorn Boonkerd Eric Giraud Neung Teaumroong A new type III effector from Bradyrhizobium sp. DOA9 encoding a putative SUMO-protease blocks nodulation in Arachis hypogaea L. Scientific Reports Bradyrhizobium sp Arachis hypogaea T3SS and SUMO-protease |
| title | A new type III effector from Bradyrhizobium sp. DOA9 encoding a putative SUMO-protease blocks nodulation in Arachis hypogaea L. |
| title_full | A new type III effector from Bradyrhizobium sp. DOA9 encoding a putative SUMO-protease blocks nodulation in Arachis hypogaea L. |
| title_fullStr | A new type III effector from Bradyrhizobium sp. DOA9 encoding a putative SUMO-protease blocks nodulation in Arachis hypogaea L. |
| title_full_unstemmed | A new type III effector from Bradyrhizobium sp. DOA9 encoding a putative SUMO-protease blocks nodulation in Arachis hypogaea L. |
| title_short | A new type III effector from Bradyrhizobium sp. DOA9 encoding a putative SUMO-protease blocks nodulation in Arachis hypogaea L. |
| title_sort | new type iii effector from bradyrhizobium sp doa9 encoding a putative sumo protease blocks nodulation in arachis hypogaea l |
| topic | Bradyrhizobium sp Arachis hypogaea T3SS and SUMO-protease |
| url | https://doi.org/10.1038/s41598-024-78913-2 |
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