Iron limitation-induced endophytic Ammoniphilus assemblage promotes root apoplastic iron remobilization by attenuation of salicylic acid pathways
Abstract Plants establish symbiotic associations with root-colonizing microbes to adapt to adverse conditions. However, how root-associated microbiota interacted with their hosts to improve plant growth under nutrient deficient conditions remains poorly understood. In this study, we explored an inte...
Saved in:
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2025-07-01
|
| Series: | npj Biofilms and Microbiomes |
| Online Access: | https://doi.org/10.1038/s41522-025-00765-z |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1849238919560822784 |
|---|---|
| author | Lin Zhu Aijing Zhang Jiansheng Guo Huabing Liu Yue Xie Xiaomin Lu Congsheng Yan Jianfei Wang Cheng Zhou |
| author_facet | Lin Zhu Aijing Zhang Jiansheng Guo Huabing Liu Yue Xie Xiaomin Lu Congsheng Yan Jianfei Wang Cheng Zhou |
| author_sort | Lin Zhu |
| collection | DOAJ |
| description | Abstract Plants establish symbiotic associations with root-colonizing microbes to adapt to adverse conditions. However, how root-associated microbiota interacted with their hosts to improve plant growth under nutrient deficient conditions remains poorly understood. In this study, we explored an interaction between tomato plants and root-associated microbiota under iron (Fe) limitation, mediated by bacterial secretion of glutamine. 16S rRNA gene sequencing revealed that Fe-limited conditions altered the composition of root-associated microbiomes, resulting in the enrichment of Ammoniphilus sp. This taxon was isolated and shown to alleviate Fe deficiency symptoms. Moreover, Fe deficiency triggered salicylic acid (SA)-induced hydrogen peroxide (H2O2) burst, thereby inhibiting the exudation of Fe-mobilizing phenolics from the roots. However, bacterial secretion of Gln greatly attenuated the SA-induced H2O2 production in the roots, thereby enhancing bacterial colonization and promoting apoplastic Fe remobilization. Collectively, these results underscored a microbial strategy for orchestrating plant SA pathways to facilitate the reutilization of root apoplastic Fe. |
| format | Article |
| id | doaj-art-c65cfe7fde134d64b48ea493bc2f44f1 |
| institution | Kabale University |
| issn | 2055-5008 |
| language | English |
| publishDate | 2025-07-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | npj Biofilms and Microbiomes |
| spelling | doaj-art-c65cfe7fde134d64b48ea493bc2f44f12025-08-20T04:01:18ZengNature Portfolionpj Biofilms and Microbiomes2055-50082025-07-0111111710.1038/s41522-025-00765-zIron limitation-induced endophytic Ammoniphilus assemblage promotes root apoplastic iron remobilization by attenuation of salicylic acid pathwaysLin Zhu0Aijing Zhang1Jiansheng Guo2Huabing Liu3Yue Xie4Xiaomin Lu5Congsheng Yan6Jianfei Wang7Cheng Zhou8Key Lab of Bio-Organic Fertilizer Creation, Ministry of Agriculture and Rural Affairs, College of Biomedicine and Health Science, Anhui Science and Technology UniversityKey Lab of Bio-Organic Fertilizer Creation, Ministry of Agriculture and Rural Affairs, College of Biomedicine and Health Science, Anhui Science and Technology UniversitySchool of Medicine, Zhejiang UniversityKey Lab of Bio-Organic Fertilizer Creation, Ministry of Agriculture and Rural Affairs, College of Biomedicine and Health Science, Anhui Science and Technology UniversityKey Lab of Bio-Organic Fertilizer Creation, Ministry of Agriculture and Rural Affairs, College of Biomedicine and Health Science, Anhui Science and Technology UniversityKey Lab of Bio-Organic Fertilizer Creation, Ministry of Agriculture and Rural Affairs, College of Biomedicine and Health Science, Anhui Science and Technology UniversityInstitute of Horticulture, Anhui Academy of Agricultural SciencesKey Lab of Bio-Organic Fertilizer Creation, Ministry of Agriculture and Rural Affairs, College of Biomedicine and Health Science, Anhui Science and Technology UniversityJiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural UniversityAbstract Plants establish symbiotic associations with root-colonizing microbes to adapt to adverse conditions. However, how root-associated microbiota interacted with their hosts to improve plant growth under nutrient deficient conditions remains poorly understood. In this study, we explored an interaction between tomato plants and root-associated microbiota under iron (Fe) limitation, mediated by bacterial secretion of glutamine. 16S rRNA gene sequencing revealed that Fe-limited conditions altered the composition of root-associated microbiomes, resulting in the enrichment of Ammoniphilus sp. This taxon was isolated and shown to alleviate Fe deficiency symptoms. Moreover, Fe deficiency triggered salicylic acid (SA)-induced hydrogen peroxide (H2O2) burst, thereby inhibiting the exudation of Fe-mobilizing phenolics from the roots. However, bacterial secretion of Gln greatly attenuated the SA-induced H2O2 production in the roots, thereby enhancing bacterial colonization and promoting apoplastic Fe remobilization. Collectively, these results underscored a microbial strategy for orchestrating plant SA pathways to facilitate the reutilization of root apoplastic Fe.https://doi.org/10.1038/s41522-025-00765-z |
| spellingShingle | Lin Zhu Aijing Zhang Jiansheng Guo Huabing Liu Yue Xie Xiaomin Lu Congsheng Yan Jianfei Wang Cheng Zhou Iron limitation-induced endophytic Ammoniphilus assemblage promotes root apoplastic iron remobilization by attenuation of salicylic acid pathways npj Biofilms and Microbiomes |
| title | Iron limitation-induced endophytic Ammoniphilus assemblage promotes root apoplastic iron remobilization by attenuation of salicylic acid pathways |
| title_full | Iron limitation-induced endophytic Ammoniphilus assemblage promotes root apoplastic iron remobilization by attenuation of salicylic acid pathways |
| title_fullStr | Iron limitation-induced endophytic Ammoniphilus assemblage promotes root apoplastic iron remobilization by attenuation of salicylic acid pathways |
| title_full_unstemmed | Iron limitation-induced endophytic Ammoniphilus assemblage promotes root apoplastic iron remobilization by attenuation of salicylic acid pathways |
| title_short | Iron limitation-induced endophytic Ammoniphilus assemblage promotes root apoplastic iron remobilization by attenuation of salicylic acid pathways |
| title_sort | iron limitation induced endophytic ammoniphilus assemblage promotes root apoplastic iron remobilization by attenuation of salicylic acid pathways |
| url | https://doi.org/10.1038/s41522-025-00765-z |
| work_keys_str_mv | AT linzhu ironlimitationinducedendophyticammoniphilusassemblagepromotesrootapoplasticironremobilizationbyattenuationofsalicylicacidpathways AT aijingzhang ironlimitationinducedendophyticammoniphilusassemblagepromotesrootapoplasticironremobilizationbyattenuationofsalicylicacidpathways AT jianshengguo ironlimitationinducedendophyticammoniphilusassemblagepromotesrootapoplasticironremobilizationbyattenuationofsalicylicacidpathways AT huabingliu ironlimitationinducedendophyticammoniphilusassemblagepromotesrootapoplasticironremobilizationbyattenuationofsalicylicacidpathways AT yuexie ironlimitationinducedendophyticammoniphilusassemblagepromotesrootapoplasticironremobilizationbyattenuationofsalicylicacidpathways AT xiaominlu ironlimitationinducedendophyticammoniphilusassemblagepromotesrootapoplasticironremobilizationbyattenuationofsalicylicacidpathways AT congshengyan ironlimitationinducedendophyticammoniphilusassemblagepromotesrootapoplasticironremobilizationbyattenuationofsalicylicacidpathways AT jianfeiwang ironlimitationinducedendophyticammoniphilusassemblagepromotesrootapoplasticironremobilizationbyattenuationofsalicylicacidpathways AT chengzhou ironlimitationinducedendophyticammoniphilusassemblagepromotesrootapoplasticironremobilizationbyattenuationofsalicylicacidpathways |