Exploring a rhizobium to fix nitrogen in non-leguminous plants by using a tumor-formation root pathogen
Abstract Over 110 million tons of nitrogen fertilizer every year is used for crop production. Scientists have dreamed of enabling rhizobial nitrogen fixation in non-leguminous crops to mitigate the increasing demand for nitrogen fertilizer. However, despite decades of research, rhizobial nitrogen fi...
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2022-12-01
|
| Series: | Phytopathology Research |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s42483-022-00154-w |
| _version_ | 1797977548264570880 |
|---|---|
| author | Ying Zhao Lixia Gao Zhixiao Gao Binnian Tian Tao Chen Jiatao Xie Jiasen Cheng Yanping Fu Youguo Li Shunyuan Xiao Ton Bisseling Daohong Jiang |
| author_facet | Ying Zhao Lixia Gao Zhixiao Gao Binnian Tian Tao Chen Jiatao Xie Jiasen Cheng Yanping Fu Youguo Li Shunyuan Xiao Ton Bisseling Daohong Jiang |
| author_sort | Ying Zhao |
| collection | DOAJ |
| description | Abstract Over 110 million tons of nitrogen fertilizer every year is used for crop production. Scientists have dreamed of enabling rhizobial nitrogen fixation in non-leguminous crops to mitigate the increasing demand for nitrogen fertilizer. However, despite decades of research, rhizobial nitrogen fixation in non-host plants has not been demonstrated. Here, we reported that an N-fixing rhizobium and a clubroot pathogen Plasmodiophora brassicae exhibited a synergistic effect on fixing nitrogen in cruciferous plants. Rhizobia were found to invade P. brassicae-infected rapeseed (Brassica napus) roots in the field. The colonization of rhizobium on rapeseed roots was confirmed by co-inoculating Mesorhizobium huakuii with P. brassicae under controlled laboratory conditions. M. huakuii infection could alleviate clubroot symptoms and promote the growth of diseased rapeseeds. M. huakuii could fix nitrogen in P. brassicae-infected plants based on the results of 15N isotope dilution tests. The expression of homologs of legume genes required for symbiosis and early-nodulin genes was significantly upregulated in Arabidopsis during early infection by P. brassicae. More importantly, M. huakuii could even fix nitrogen in P. brassicae-resistant rapeseed cultivar and promote plant growth when co-inoculated with P. brassicae. Our findings provide a new avenue to understand the interaction of rhizobia with non-host plants, stimulate the exploration of fixing nitrogen in non-leguminous plants by nitrogen-fixing rhizobia, and develop a strategy for both disease control and nitrogen fixation on non-host crops. |
| first_indexed | 2024-04-11T05:09:47Z |
| format | Article |
| id | doaj.art-8b93f64b6f524bbe85abf0ad0d8a8a7c |
| institution | Directory Open Access Journal |
| issn | 2524-4167 |
| language | English |
| last_indexed | 2024-04-11T05:09:47Z |
| publishDate | 2022-12-01 |
| publisher | BMC |
| record_format | Article |
| series | Phytopathology Research |
| spelling | doaj.art-8b93f64b6f524bbe85abf0ad0d8a8a7c2022-12-25T12:06:50ZengBMCPhytopathology Research2524-41672022-12-014111410.1186/s42483-022-00154-wExploring a rhizobium to fix nitrogen in non-leguminous plants by using a tumor-formation root pathogenYing Zhao0Lixia Gao1Zhixiao Gao2Binnian Tian3Tao Chen4Jiatao Xie5Jiasen Cheng6Yanping Fu7Youguo Li8Shunyuan Xiao9Ton Bisseling10Daohong Jiang11State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityState Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityDepartment of Plant Science and Landscape Architecture, Institute for Bioscience and Biotechnology Research, University of MarylandLaboratory of Molecular Biology, Department of Plant Science, Wageningen UniversityState Key Laboratory of Agricultural Microbiology, Huazhong Agricultural UniversityAbstract Over 110 million tons of nitrogen fertilizer every year is used for crop production. Scientists have dreamed of enabling rhizobial nitrogen fixation in non-leguminous crops to mitigate the increasing demand for nitrogen fertilizer. However, despite decades of research, rhizobial nitrogen fixation in non-host plants has not been demonstrated. Here, we reported that an N-fixing rhizobium and a clubroot pathogen Plasmodiophora brassicae exhibited a synergistic effect on fixing nitrogen in cruciferous plants. Rhizobia were found to invade P. brassicae-infected rapeseed (Brassica napus) roots in the field. The colonization of rhizobium on rapeseed roots was confirmed by co-inoculating Mesorhizobium huakuii with P. brassicae under controlled laboratory conditions. M. huakuii infection could alleviate clubroot symptoms and promote the growth of diseased rapeseeds. M. huakuii could fix nitrogen in P. brassicae-infected plants based on the results of 15N isotope dilution tests. The expression of homologs of legume genes required for symbiosis and early-nodulin genes was significantly upregulated in Arabidopsis during early infection by P. brassicae. More importantly, M. huakuii could even fix nitrogen in P. brassicae-resistant rapeseed cultivar and promote plant growth when co-inoculated with P. brassicae. Our findings provide a new avenue to understand the interaction of rhizobia with non-host plants, stimulate the exploration of fixing nitrogen in non-leguminous plants by nitrogen-fixing rhizobia, and develop a strategy for both disease control and nitrogen fixation on non-host crops.https://doi.org/10.1186/s42483-022-00154-wRhizobiaNitrogen fixationNon-leguminous plantsBrassica napusPlant pathogenPlasmodiophora brassicae |
| spellingShingle | Ying Zhao Lixia Gao Zhixiao Gao Binnian Tian Tao Chen Jiatao Xie Jiasen Cheng Yanping Fu Youguo Li Shunyuan Xiao Ton Bisseling Daohong Jiang Exploring a rhizobium to fix nitrogen in non-leguminous plants by using a tumor-formation root pathogen Phytopathology Research Rhizobia Nitrogen fixation Non-leguminous plants Brassica napus Plant pathogen Plasmodiophora brassicae |
| title | Exploring a rhizobium to fix nitrogen in non-leguminous plants by using a tumor-formation root pathogen |
| title_full | Exploring a rhizobium to fix nitrogen in non-leguminous plants by using a tumor-formation root pathogen |
| title_fullStr | Exploring a rhizobium to fix nitrogen in non-leguminous plants by using a tumor-formation root pathogen |
| title_full_unstemmed | Exploring a rhizobium to fix nitrogen in non-leguminous plants by using a tumor-formation root pathogen |
| title_short | Exploring a rhizobium to fix nitrogen in non-leguminous plants by using a tumor-formation root pathogen |
| title_sort | exploring a rhizobium to fix nitrogen in non leguminous plants by using a tumor formation root pathogen |
| topic | Rhizobia Nitrogen fixation Non-leguminous plants Brassica napus Plant pathogen Plasmodiophora brassicae |
| url | https://doi.org/10.1186/s42483-022-00154-w |
| work_keys_str_mv | AT yingzhao exploringarhizobiumtofixnitrogeninnonleguminousplantsbyusingatumorformationrootpathogen AT lixiagao exploringarhizobiumtofixnitrogeninnonleguminousplantsbyusingatumorformationrootpathogen AT zhixiaogao exploringarhizobiumtofixnitrogeninnonleguminousplantsbyusingatumorformationrootpathogen AT binniantian exploringarhizobiumtofixnitrogeninnonleguminousplantsbyusingatumorformationrootpathogen AT taochen exploringarhizobiumtofixnitrogeninnonleguminousplantsbyusingatumorformationrootpathogen AT jiataoxie exploringarhizobiumtofixnitrogeninnonleguminousplantsbyusingatumorformationrootpathogen AT jiasencheng exploringarhizobiumtofixnitrogeninnonleguminousplantsbyusingatumorformationrootpathogen AT yanpingfu exploringarhizobiumtofixnitrogeninnonleguminousplantsbyusingatumorformationrootpathogen AT youguoli exploringarhizobiumtofixnitrogeninnonleguminousplantsbyusingatumorformationrootpathogen AT shunyuanxiao exploringarhizobiumtofixnitrogeninnonleguminousplantsbyusingatumorformationrootpathogen AT tonbisseling exploringarhizobiumtofixnitrogeninnonleguminousplantsbyusingatumorformationrootpathogen AT daohongjiang exploringarhizobiumtofixnitrogeninnonleguminousplantsbyusingatumorformationrootpathogen |