Biotic and Abiotic Stress Factors Induce Microbiome Shifts and Enrichment of Distinct Beneficial Bacteria in Tomato Roots
Crops are often simultaneously threatened by abiotic and biotic stress factors but the stress response of the plant holobiont is not well understood, despite the high importance of this response to ensure future plant production. Therefore, the aim of this study was to assess the impact of individua...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
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The American Phytopathological Society
2022-12-01
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| Series: | Phytobiomes Journal |
| Subjects: | |
| Online Access: | https://apsjournals.apsnet.org/doi/10.1094/PBIOMES-10-21-0067-R |
| _version_ | 1828088125908320256 |
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| author | Burkhardt Flemer Sneha Gulati Alessandro Bergna Manuela Rändler Tomislav Cernava Katja Witzel Gabriele Berg Rita Grosch |
| author_facet | Burkhardt Flemer Sneha Gulati Alessandro Bergna Manuela Rändler Tomislav Cernava Katja Witzel Gabriele Berg Rita Grosch |
| author_sort | Burkhardt Flemer |
| collection | DOAJ |
| description | Crops are often simultaneously threatened by abiotic and biotic stress factors but the stress response of the plant holobiont is not well understood, despite the high importance of this response to ensure future plant production. Therefore, the aim of this study was to assess the impact of individual and combined abiotic (ionic and osmotic) and biotic (Verticillium dahliae and Fusarium oxysporum) stress factors on plant performance and on the bacterial composition of the root endosphere in tomato. Structure and function of the microbiota was analyzed by 16S ribosomal RNA gene amplicon sequencing and a complementary cultivation approach, including in vitro and in vivo assays. Under all stress conditions, tomato growth and photosynthetic activity was reduced. Combined abiotic stressors with F. oxysporum but not with V. dahliae infection led to an additive negative effect on plant performance. All stress conditions induced a microbiome shift, and changed the relative abundance of phyla such as Firmicutes and classes of Proteobacteria. Endophytes identified as Bacillus, Paenibacillus, and Microbacterium spp. showed tolerance to abiotic stress conditions and plant beneficial effects. Stressor-specific enrichments of beneficial bacteria in the root were discovered (e.g., Paenibacillus in roots infected with F. oxysporum and Microbacterium in roots infected with V. dahliae). Interestingly, endophytes that were able to promote plant growth were obtained only from roots exposed to individual biotic and combined abiotic and biotic stress conditions but not individual abiotic stressors. Our study revealed stressor-specific enrichment of beneficial bacteria in tomato roots, which has implications for novel plant protection strategies. |
| first_indexed | 2024-04-11T05:21:45Z |
| format | Article |
| id | doaj.art-732392d4f18c491eae0c3517431d36db |
| institution | Directory Open Access Journal |
| issn | 2471-2906 |
| language | English |
| last_indexed | 2024-04-11T05:21:45Z |
| publishDate | 2022-12-01 |
| publisher | The American Phytopathological Society |
| record_format | Article |
| series | Phytobiomes Journal |
| spelling | doaj.art-732392d4f18c491eae0c3517431d36db2022-12-23T17:00:45ZengThe American Phytopathological SocietyPhytobiomes Journal2471-29062022-12-016427628910.1094/PBIOMES-10-21-0067-RBiotic and Abiotic Stress Factors Induce Microbiome Shifts and Enrichment of Distinct Beneficial Bacteria in Tomato RootsBurkhardt Flemer0Sneha Gulati1Alessandro Bergna2Manuela Rändler3Tomislav Cernava4Katja Witzel5Gabriele Berg6Rita Grosch7Leibniz Institute of Vegetable and Ornamental Crops (IGZ) e.V., Plant-Microbe Systems Grossbeeren, GermanyLeibniz Institute of Vegetable and Ornamental Crops (IGZ) e.V., Plant-Microbe Systems Grossbeeren, GermanyGraz University of Technology, Institute of Environmental Biotechnology, Graz, AustriaGraz University of Technology, Institute of Environmental Biotechnology, Graz, AustriaGraz University of Technology, Institute of Environmental Biotechnology, Graz, AustriaLeibniz Institute of Vegetable and Ornamental Crops (IGZ) e.V., Plant-Microbe Systems Grossbeeren, GermanyGraz University of Technology, Institute of Environmental Biotechnology, Graz, AustriaLeibniz Institute of Vegetable and Ornamental Crops (IGZ) e.V., Plant-Microbe Systems Grossbeeren, GermanyCrops are often simultaneously threatened by abiotic and biotic stress factors but the stress response of the plant holobiont is not well understood, despite the high importance of this response to ensure future plant production. Therefore, the aim of this study was to assess the impact of individual and combined abiotic (ionic and osmotic) and biotic (Verticillium dahliae and Fusarium oxysporum) stress factors on plant performance and on the bacterial composition of the root endosphere in tomato. Structure and function of the microbiota was analyzed by 16S ribosomal RNA gene amplicon sequencing and a complementary cultivation approach, including in vitro and in vivo assays. Under all stress conditions, tomato growth and photosynthetic activity was reduced. Combined abiotic stressors with F. oxysporum but not with V. dahliae infection led to an additive negative effect on plant performance. All stress conditions induced a microbiome shift, and changed the relative abundance of phyla such as Firmicutes and classes of Proteobacteria. Endophytes identified as Bacillus, Paenibacillus, and Microbacterium spp. showed tolerance to abiotic stress conditions and plant beneficial effects. Stressor-specific enrichments of beneficial bacteria in the root were discovered (e.g., Paenibacillus in roots infected with F. oxysporum and Microbacterium in roots infected with V. dahliae). Interestingly, endophytes that were able to promote plant growth were obtained only from roots exposed to individual biotic and combined abiotic and biotic stress conditions but not individual abiotic stressors. Our study revealed stressor-specific enrichment of beneficial bacteria in tomato roots, which has implications for novel plant protection strategies.https://apsjournals.apsnet.org/doi/10.1094/PBIOMES-10-21-0067-Rcombined stress factorsFusariummicrobiomeosmotic stresssalinitysoilborne pathogens |
| spellingShingle | Burkhardt Flemer Sneha Gulati Alessandro Bergna Manuela Rändler Tomislav Cernava Katja Witzel Gabriele Berg Rita Grosch Biotic and Abiotic Stress Factors Induce Microbiome Shifts and Enrichment of Distinct Beneficial Bacteria in Tomato Roots Phytobiomes Journal combined stress factors Fusarium microbiome osmotic stress salinity soilborne pathogens |
| title | Biotic and Abiotic Stress Factors Induce Microbiome Shifts and Enrichment of Distinct Beneficial Bacteria in Tomato Roots |
| title_full | Biotic and Abiotic Stress Factors Induce Microbiome Shifts and Enrichment of Distinct Beneficial Bacteria in Tomato Roots |
| title_fullStr | Biotic and Abiotic Stress Factors Induce Microbiome Shifts and Enrichment of Distinct Beneficial Bacteria in Tomato Roots |
| title_full_unstemmed | Biotic and Abiotic Stress Factors Induce Microbiome Shifts and Enrichment of Distinct Beneficial Bacteria in Tomato Roots |
| title_short | Biotic and Abiotic Stress Factors Induce Microbiome Shifts and Enrichment of Distinct Beneficial Bacteria in Tomato Roots |
| title_sort | biotic and abiotic stress factors induce microbiome shifts and enrichment of distinct beneficial bacteria in tomato roots |
| topic | combined stress factors Fusarium microbiome osmotic stress salinity soilborne pathogens |
| url | https://apsjournals.apsnet.org/doi/10.1094/PBIOMES-10-21-0067-R |
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