Involvement of a Novel TetR-Like Regulator (BdtR) of Bradyrhizobium diazoefficiens in the Efflux of Isoflavonoid Genistein
A wide variety of leguminous plant-released (iso)flavonoids, such as genistein, are potential inducers of the nodulation (nod) genes of endosymbiotic rhizobia for the production of Nod factors, which are vital signaling molecules for triggering the symbiotic process. However, these (iso)flavonoids a...
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| Format: | Article |
| Language: | English |
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The American Phytopathological Society
2020-12-01
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| Series: | Molecular Plant-Microbe Interactions |
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| Online Access: | https://apsjournals.apsnet.org/doi/10.1094/MPMI-08-20-0243-R |
| _version_ | 1818915216582246400 |
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| author | Fang Han Xueqian He Wenwen Chen Haoyu Gai Xuemei Bai Yongxing He Keisuke Takeshima Takuji Ohwada Min Wei Fang Xie |
| author_facet | Fang Han Xueqian He Wenwen Chen Haoyu Gai Xuemei Bai Yongxing He Keisuke Takeshima Takuji Ohwada Min Wei Fang Xie |
| author_sort | Fang Han |
| collection | DOAJ |
| description | A wide variety of leguminous plant-released (iso)flavonoids, such as genistein, are potential inducers of the nodulation (nod) genes of endosymbiotic rhizobia for the production of Nod factors, which are vital signaling molecules for triggering the symbiotic process. However, these (iso)flavonoids are generally thought to be toxic to the bacterial partner to varying degrees. Here, a novel TetR-like regulator gene of the soybean symbiont Bradyrhizobium diazoefficiens USDA110, bdtR (systematic designation blr7023), was characterized. It was found to be rapidly and preferentially induced by genistein, and its mutation resulted in significantly increased expression of the neighboring bll7019-bll7021 genes, encoding a multidrug resistance efflux pump system, in the absence of this isoflavonoid. Then, the transcriptional start site of BdtR was determined, and it was revealed that BdtR acted as a transcriptional repressor of the above efflux system through the binding of an AT-rich operator, which could be completely prevented by genistein. In addition, the ΔbdtR deletion mutant strain showed higher accumulation of extracellular genistein and became less susceptible to the isoflavonoid. In contrast, the inactivation of BdtR led to the significantly decreased induction of a nodulation gene (nodY) independent of the expression of nodD1 and nodW and to much weaker nodulation competitiveness. Taken together, the results show that BdtR plays an early sensing role in maintaining the intracellular homeostasis of genistein, helping to alleviate its toxic effect on this bacterium by negatively regulating neighboring genes encoding an efflux pump system while being essentially required for nodule occupancy competitiveness.[Graphic: see text] Copyright © 2020 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license. |
| first_indexed | 2024-12-19T23:58:45Z |
| format | Article |
| id | doaj.art-2fc1993c92dc40e5b5b4319cc36b9f79 |
| institution | Directory Open Access Journal |
| issn | 0894-0282 1943-7706 |
| language | English |
| last_indexed | 2024-12-19T23:58:45Z |
| publishDate | 2020-12-01 |
| publisher | The American Phytopathological Society |
| record_format | Article |
| series | Molecular Plant-Microbe Interactions |
| spelling | doaj.art-2fc1993c92dc40e5b5b4319cc36b9f792022-12-21T20:00:55ZengThe American Phytopathological SocietyMolecular Plant-Microbe Interactions0894-02821943-77062020-12-0133121411142310.1094/MPMI-08-20-0243-RInvolvement of a Novel TetR-Like Regulator (BdtR) of Bradyrhizobium diazoefficiens in the Efflux of Isoflavonoid GenisteinFang Han0Xueqian He1Wenwen Chen2Haoyu Gai3Xuemei Bai4Yongxing He5Keisuke Takeshima6Takuji Ohwada7Min Wei8Fang Xie9State Key Laboratory of Grassland Agro-Ecosystems, Institute of Arid Agroecology, School of Life Sciences, Lanzhou University, No. 222, South Tianshui Road, Lanzhou 730000, ChinaState Key Laboratory of Grassland Agro-Ecosystems, Institute of Arid Agroecology, School of Life Sciences, Lanzhou University, No. 222, South Tianshui Road, Lanzhou 730000, ChinaState Key Laboratory of Grassland Agro-Ecosystems, Institute of Arid Agroecology, School of Life Sciences, Lanzhou University, No. 222, South Tianshui Road, Lanzhou 730000, ChinaState Key Laboratory of Grassland Agro-Ecosystems, Institute of Arid Agroecology, School of Life Sciences, Lanzhou University, No. 222, South Tianshui Road, Lanzhou 730000, ChinaState Key Laboratory of Grassland Agro-Ecosystems, Institute of Arid Agroecology, School of Life Sciences, Lanzhou University, No. 222, South Tianshui Road, Lanzhou 730000, ChinaState Key Laboratory of Grassland Agro-Ecosystems, Institute of Arid Agroecology, School of Life Sciences, Lanzhou University, No. 222, South Tianshui Road, Lanzhou 730000, ChinaDepartment of Food Science, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido 080-8555, JapanDepartment of Food Science, Obihiro University of Agriculture and Veterinary Medicine, Obihiro, Hokkaido 080-8555, JapanState Key Laboratory of Grassland Agro-Ecosystems, Institute of Arid Agroecology, School of Life Sciences, Lanzhou University, No. 222, South Tianshui Road, Lanzhou 730000, ChinaNational Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, ChinaA wide variety of leguminous plant-released (iso)flavonoids, such as genistein, are potential inducers of the nodulation (nod) genes of endosymbiotic rhizobia for the production of Nod factors, which are vital signaling molecules for triggering the symbiotic process. However, these (iso)flavonoids are generally thought to be toxic to the bacterial partner to varying degrees. Here, a novel TetR-like regulator gene of the soybean symbiont Bradyrhizobium diazoefficiens USDA110, bdtR (systematic designation blr7023), was characterized. It was found to be rapidly and preferentially induced by genistein, and its mutation resulted in significantly increased expression of the neighboring bll7019-bll7021 genes, encoding a multidrug resistance efflux pump system, in the absence of this isoflavonoid. Then, the transcriptional start site of BdtR was determined, and it was revealed that BdtR acted as a transcriptional repressor of the above efflux system through the binding of an AT-rich operator, which could be completely prevented by genistein. In addition, the ΔbdtR deletion mutant strain showed higher accumulation of extracellular genistein and became less susceptible to the isoflavonoid. In contrast, the inactivation of BdtR led to the significantly decreased induction of a nodulation gene (nodY) independent of the expression of nodD1 and nodW and to much weaker nodulation competitiveness. Taken together, the results show that BdtR plays an early sensing role in maintaining the intracellular homeostasis of genistein, helping to alleviate its toxic effect on this bacterium by negatively regulating neighboring genes encoding an efflux pump system while being essentially required for nodule occupancy competitiveness.[Graphic: see text] Copyright © 2020 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.https://apsjournals.apsnet.org/doi/10.1094/MPMI-08-20-0243-RBradyrhizobium diazoefficiensisoflavonoidgenisteinefflux pumpnodulation competitiveness |
| spellingShingle | Fang Han Xueqian He Wenwen Chen Haoyu Gai Xuemei Bai Yongxing He Keisuke Takeshima Takuji Ohwada Min Wei Fang Xie Involvement of a Novel TetR-Like Regulator (BdtR) of Bradyrhizobium diazoefficiens in the Efflux of Isoflavonoid Genistein Molecular Plant-Microbe Interactions Bradyrhizobium diazoefficiens isoflavonoid genistein efflux pump nodulation competitiveness |
| title | Involvement of a Novel TetR-Like Regulator (BdtR) of Bradyrhizobium diazoefficiens in the Efflux of Isoflavonoid Genistein |
| title_full | Involvement of a Novel TetR-Like Regulator (BdtR) of Bradyrhizobium diazoefficiens in the Efflux of Isoflavonoid Genistein |
| title_fullStr | Involvement of a Novel TetR-Like Regulator (BdtR) of Bradyrhizobium diazoefficiens in the Efflux of Isoflavonoid Genistein |
| title_full_unstemmed | Involvement of a Novel TetR-Like Regulator (BdtR) of Bradyrhizobium diazoefficiens in the Efflux of Isoflavonoid Genistein |
| title_short | Involvement of a Novel TetR-Like Regulator (BdtR) of Bradyrhizobium diazoefficiens in the Efflux of Isoflavonoid Genistein |
| title_sort | involvement of a novel tetr like regulator bdtr of bradyrhizobium diazoefficiens in the efflux of isoflavonoid genistein |
| topic | Bradyrhizobium diazoefficiens isoflavonoid genistein efflux pump nodulation competitiveness |
| url | https://apsjournals.apsnet.org/doi/10.1094/MPMI-08-20-0243-R |
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