<i>Sinorhizobium fredii</i> HH103 RirA Is Required for Oxidative Stress Resistance and Efficient Symbiosis with Soybean
Members of <i>Rhizobiaceae</i> contain a homologue of the iron-responsive regulatory protein RirA. In different bacteria, RirA acts as a repressor of iron uptake systems under iron-replete conditions and contributes to ameliorate cell damage during oxidative stress. In <i>Rhizobium...
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| Format: | Article |
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MDPI AG
2019-02-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/20/3/787 |
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| author | Juan Carlos Crespo-Rivas Pilar Navarro-Gómez Cynthia Alias-Villegas Jie Shi Tao Zhen Yanbo Niu Virginia Cuéllar Javier Moreno Teresa Cubo José María Vinardell José Enrique Ruiz-Sainz Sebastián Acosta-Jurado María José Soto |
| author_facet | Juan Carlos Crespo-Rivas Pilar Navarro-Gómez Cynthia Alias-Villegas Jie Shi Tao Zhen Yanbo Niu Virginia Cuéllar Javier Moreno Teresa Cubo José María Vinardell José Enrique Ruiz-Sainz Sebastián Acosta-Jurado María José Soto |
| author_sort | Juan Carlos Crespo-Rivas |
| collection | DOAJ |
| description | Members of <i>Rhizobiaceae</i> contain a homologue of the iron-responsive regulatory protein RirA. In different bacteria, RirA acts as a repressor of iron uptake systems under iron-replete conditions and contributes to ameliorate cell damage during oxidative stress. In <i>Rhizobium leguminosarum</i> and <i>Sinorhizobium meliloti</i>, mutations in <i>rirA</i> do not impair symbiotic nitrogen fixation. In this study, a <i>rirA</i> mutant of broad host range <i>S. fredii</i> HH103 has been constructed (SVQ780) and its free-living and symbiotic phenotypes evaluated. No production of siderophores could be detected in either the wild-type or SVQ780. The <i>rirA</i> mutant exhibited a growth advantage under iron-deficient conditions and hypersensitivity to hydrogen peroxide in iron-rich medium. Transcription of <i>rirA</i> in HH103 is subject to autoregulation and inactivation of the gene upregulates <i>fbpA</i>, a gene putatively involved in iron transport. The <i>S. fredii rirA</i> mutant was able to nodulate soybean plants, but symbiotic nitrogen fixation was impaired. Nodules induced by the mutant were poorly infected compared to those induced by the wild-type. Genetic complementation reversed the mutant’s hypersensitivity to H<sub>2</sub>O<sub>2</sub>, expression of <i>fbpA</i>, and symbiotic deficiency in soybean plants. This is the first report that demonstrates a role for RirA in the <i>Rhizobium</i>-legume symbiosis. |
| first_indexed | 2024-04-12T06:50:11Z |
| format | Article |
| id | doaj.art-490d9abdd8a4452b86f63f63b2dbc418 |
| institution | Directory Open Access Journal |
| issn | 1422-0067 |
| language | English |
| last_indexed | 2024-04-12T06:50:11Z |
| publishDate | 2019-02-01 |
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| series | International Journal of Molecular Sciences |
| spelling | doaj.art-490d9abdd8a4452b86f63f63b2dbc4182022-12-22T03:43:21ZengMDPI AGInternational Journal of Molecular Sciences1422-00672019-02-0120378710.3390/ijms20030787ijms20030787<i>Sinorhizobium fredii</i> HH103 RirA Is Required for Oxidative Stress Resistance and Efficient Symbiosis with SoybeanJuan Carlos Crespo-Rivas0Pilar Navarro-Gómez1Cynthia Alias-Villegas2Jie Shi3Tao Zhen4Yanbo Niu5Virginia Cuéllar6Javier Moreno7Teresa Cubo8José María Vinardell9José Enrique Ruiz-Sainz10Sebastián Acosta-Jurado11María José Soto12Departamento de Microbiología, Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012 Sevilla, SpainDepartamento de Microbiología, Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012 Sevilla, SpainDepartamento de Microbiología, Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012 Sevilla, SpainDaqing Branch of Heilongjiang Academy of Sciences, Daqing 163000, ChinaInstitute of Microbiology, Heilongjiang Academy of Sciences, Harbin 150001, ChinaInstitute of Microbiology, Heilongjiang Academy of Sciences, Harbin 150001, ChinaDepartamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín, CSIC, c/ Profesor Albareda 1, 18008 Granada, SpainDepartamento de Biología Celular, Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012 Sevilla, SpainDepartamento de Microbiología, Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012 Sevilla, SpainDepartamento de Microbiología, Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012 Sevilla, SpainDepartamento de Microbiología, Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012 Sevilla, SpainDepartamento de Microbiología, Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012 Sevilla, SpainDepartamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín, CSIC, c/ Profesor Albareda 1, 18008 Granada, SpainMembers of <i>Rhizobiaceae</i> contain a homologue of the iron-responsive regulatory protein RirA. In different bacteria, RirA acts as a repressor of iron uptake systems under iron-replete conditions and contributes to ameliorate cell damage during oxidative stress. In <i>Rhizobium leguminosarum</i> and <i>Sinorhizobium meliloti</i>, mutations in <i>rirA</i> do not impair symbiotic nitrogen fixation. In this study, a <i>rirA</i> mutant of broad host range <i>S. fredii</i> HH103 has been constructed (SVQ780) and its free-living and symbiotic phenotypes evaluated. No production of siderophores could be detected in either the wild-type or SVQ780. The <i>rirA</i> mutant exhibited a growth advantage under iron-deficient conditions and hypersensitivity to hydrogen peroxide in iron-rich medium. Transcription of <i>rirA</i> in HH103 is subject to autoregulation and inactivation of the gene upregulates <i>fbpA</i>, a gene putatively involved in iron transport. The <i>S. fredii rirA</i> mutant was able to nodulate soybean plants, but symbiotic nitrogen fixation was impaired. Nodules induced by the mutant were poorly infected compared to those induced by the wild-type. Genetic complementation reversed the mutant’s hypersensitivity to H<sub>2</sub>O<sub>2</sub>, expression of <i>fbpA</i>, and symbiotic deficiency in soybean plants. This is the first report that demonstrates a role for RirA in the <i>Rhizobium</i>-legume symbiosis.https://www.mdpi.com/1422-0067/20/3/787iron<i>Rhizobium</i>regulationsiderophorenitrogen-fixationplant–bacteria interaction |
| spellingShingle | Juan Carlos Crespo-Rivas Pilar Navarro-Gómez Cynthia Alias-Villegas Jie Shi Tao Zhen Yanbo Niu Virginia Cuéllar Javier Moreno Teresa Cubo José María Vinardell José Enrique Ruiz-Sainz Sebastián Acosta-Jurado María José Soto <i>Sinorhizobium fredii</i> HH103 RirA Is Required for Oxidative Stress Resistance and Efficient Symbiosis with Soybean International Journal of Molecular Sciences iron <i>Rhizobium</i> regulation siderophore nitrogen-fixation plant–bacteria interaction |
| title | <i>Sinorhizobium fredii</i> HH103 RirA Is Required for Oxidative Stress Resistance and Efficient Symbiosis with Soybean |
| title_full | <i>Sinorhizobium fredii</i> HH103 RirA Is Required for Oxidative Stress Resistance and Efficient Symbiosis with Soybean |
| title_fullStr | <i>Sinorhizobium fredii</i> HH103 RirA Is Required for Oxidative Stress Resistance and Efficient Symbiosis with Soybean |
| title_full_unstemmed | <i>Sinorhizobium fredii</i> HH103 RirA Is Required for Oxidative Stress Resistance and Efficient Symbiosis with Soybean |
| title_short | <i>Sinorhizobium fredii</i> HH103 RirA Is Required for Oxidative Stress Resistance and Efficient Symbiosis with Soybean |
| title_sort | i sinorhizobium fredii i hh103 rira is required for oxidative stress resistance and efficient symbiosis with soybean |
| topic | iron <i>Rhizobium</i> regulation siderophore nitrogen-fixation plant–bacteria interaction |
| url | https://www.mdpi.com/1422-0067/20/3/787 |
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