Distinct microbiota assembly and functional patterns in disease-resistant and susceptible varieties of tobacco
The plant microbiota is believed to be an accessory genome that extends plant functions, forming holobionts together with the host plant. Plant disease resistance, therefore, is inextricably linked with plant microbiota, which play important roles in plant growth and health. To explore the relations...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2024-03-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2024.1361883/full |
| _version_ | 1797289731422158848 |
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| author | Luhua Yang Luhua Yang Yuan Guo Hui Yang Hui Yang Hui Yang Shun Li Shun Li Yunzeng Zhang Cheng Gao Tian Wei Likai Hao Likai Hao Likai Hao |
| author_facet | Luhua Yang Luhua Yang Yuan Guo Hui Yang Hui Yang Hui Yang Shun Li Shun Li Yunzeng Zhang Cheng Gao Tian Wei Likai Hao Likai Hao Likai Hao |
| author_sort | Luhua Yang |
| collection | DOAJ |
| description | The plant microbiota is believed to be an accessory genome that extends plant functions, forming holobionts together with the host plant. Plant disease resistance, therefore, is inextricably linked with plant microbiota, which play important roles in plant growth and health. To explore the relationship between plant microbiota and disease resistance, we investigated the tobacco microbiome of two varieties with contrasting disease-resistance levels to bacterial wilt and black shank diseases. Comparative microbiome analysis indicated that the resistant variety assembled a distinct microbiota with higher network complexity and diversity. While Pseudomonas and Ensifer, which contain biocontrol and beneficial members, were enriched in the rhizosphere of the resistant variety, Ralstonia, a genus including the known causative pathogen, was enriched in the susceptible variety. Metagenome sequencing revealed that biocontrol functions, such as hydrogen cyanide synthase, pyochelin biosynthesis, and arthrofactin-type cyclic lipopeptide synthetase, were more abundant in the resistant variety. Further analysis indicated that contigs encoding the corresponding genes were mostly assigned to Pseudomonas. Among all the metagenome-assembled genomes, positive selection was suggested in the genome assigned to Pseudomonas only in the rhizosphere of the resistant variety. The search of biosynthetic gene clusters in the Pseudomonas genome revealed a non-ribosomal peptide synthetase, the compound of which was brabantamide A, with known antimicrobial activity. Collectively, our study suggests that the plant microbiota might be involved in microbe-mediated disease resistance. Particularly, our results highlight Pseudomonas in the rhizosphere of the disease-resistant variety as a promising biocontrol candidate. Our study may facilitate further screening of bacterial isolates and the targeted design of microbial communities. |
| first_indexed | 2024-03-07T19:10:16Z |
| format | Article |
| id | doaj.art-4c49fe2099654de99c0f6f9128eb414b |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-03-07T19:10:16Z |
| publishDate | 2024-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-4c49fe2099654de99c0f6f9128eb414b2024-03-01T04:57:22ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-03-011510.3389/fmicb.2024.13618831361883Distinct microbiota assembly and functional patterns in disease-resistant and susceptible varieties of tobaccoLuhua Yang0Luhua Yang1Yuan Guo2Hui Yang3Hui Yang4Hui Yang5Shun Li6Shun Li7Yunzeng Zhang8Cheng Gao9Tian Wei10Likai Hao11Likai Hao12Likai Hao13Key Laboratory of Marine Environmental Corrosion and Biofouling, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, ChinaKey Laboratory of Urban Environment and Health, Ningbo Urban Environment Observation and Research Station, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, ChinaState Key Laboratory of Environmental Geochemistry, Institute of Geochemistry, Chinese Academy of Sciences, Guiyang, ChinaState Key Laboratory of Environmental Geochemistry, Institute of Geochemistry, Chinese Academy of Sciences, Guiyang, ChinaGuizhou Academy of Tobacco Science, Guiyang, ChinaUniversity of Chinese Academy of Sciences, Beijing, ChinaKey Laboratory of Urban Environment and Health, Ningbo Urban Environment Observation and Research Station, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, ChinaZhejiang Key Laboratory of Urban Environmental Processes and Pollution Control, CAS Haixi Industrial Technology Innovation Center in Beilun, Ningbo, ChinaCollege of Bioscience and Biotechnology, Yangzhou University, Yangzhou, ChinaState Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing, ChinaBei Bu Zhan Qu CDC, Shenyang, ChinaState Key Laboratory of Environmental Geochemistry, Institute of Geochemistry, Chinese Academy of Sciences, Guiyang, ChinaUniversity of Chinese Academy of Sciences, Beijing, China0CAS Center for Excellence in Quaternary Science and Global Change, Xi’an, ChinaThe plant microbiota is believed to be an accessory genome that extends plant functions, forming holobionts together with the host plant. Plant disease resistance, therefore, is inextricably linked with plant microbiota, which play important roles in plant growth and health. To explore the relationship between plant microbiota and disease resistance, we investigated the tobacco microbiome of two varieties with contrasting disease-resistance levels to bacterial wilt and black shank diseases. Comparative microbiome analysis indicated that the resistant variety assembled a distinct microbiota with higher network complexity and diversity. While Pseudomonas and Ensifer, which contain biocontrol and beneficial members, were enriched in the rhizosphere of the resistant variety, Ralstonia, a genus including the known causative pathogen, was enriched in the susceptible variety. Metagenome sequencing revealed that biocontrol functions, such as hydrogen cyanide synthase, pyochelin biosynthesis, and arthrofactin-type cyclic lipopeptide synthetase, were more abundant in the resistant variety. Further analysis indicated that contigs encoding the corresponding genes were mostly assigned to Pseudomonas. Among all the metagenome-assembled genomes, positive selection was suggested in the genome assigned to Pseudomonas only in the rhizosphere of the resistant variety. The search of biosynthetic gene clusters in the Pseudomonas genome revealed a non-ribosomal peptide synthetase, the compound of which was brabantamide A, with known antimicrobial activity. Collectively, our study suggests that the plant microbiota might be involved in microbe-mediated disease resistance. Particularly, our results highlight Pseudomonas in the rhizosphere of the disease-resistant variety as a promising biocontrol candidate. Our study may facilitate further screening of bacterial isolates and the targeted design of microbial communities.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1361883/fullplant microbiotatobacco microbiomedisease resistancepositive selectionbiocontrol |
| spellingShingle | Luhua Yang Luhua Yang Yuan Guo Hui Yang Hui Yang Hui Yang Shun Li Shun Li Yunzeng Zhang Cheng Gao Tian Wei Likai Hao Likai Hao Likai Hao Distinct microbiota assembly and functional patterns in disease-resistant and susceptible varieties of tobacco Frontiers in Microbiology plant microbiota tobacco microbiome disease resistance positive selection biocontrol |
| title | Distinct microbiota assembly and functional patterns in disease-resistant and susceptible varieties of tobacco |
| title_full | Distinct microbiota assembly and functional patterns in disease-resistant and susceptible varieties of tobacco |
| title_fullStr | Distinct microbiota assembly and functional patterns in disease-resistant and susceptible varieties of tobacco |
| title_full_unstemmed | Distinct microbiota assembly and functional patterns in disease-resistant and susceptible varieties of tobacco |
| title_short | Distinct microbiota assembly and functional patterns in disease-resistant and susceptible varieties of tobacco |
| title_sort | distinct microbiota assembly and functional patterns in disease resistant and susceptible varieties of tobacco |
| topic | plant microbiota tobacco microbiome disease resistance positive selection biocontrol |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2024.1361883/full |
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