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Patterns in the Microbial Community of Salt-Tolerant Plants and the Functional Genes Associated with Salt Stress Alleviation
Salinity is an important abiotic stress affecting plant growth. We have known that plants can recruit beneficial microbes from the surrounding soil. However, the ecological functions of the core microbiome in salt-tolerant plants, together with their driving factors, remain largely unexplored. Here,...
Autores principales: | , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8549722/ https://www.ncbi.nlm.nih.gov/pubmed/34704793 http://dx.doi.org/10.1128/Spectrum.00767-21 |
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author | Zheng, Yanfen Xu, Zongchang Liu, Haodong Liu, Yan Zhou, Yanan Meng, Chen Ma, Siqi Xie, Zhihong Li, Yiqiang Zhang, Cheng-Sheng |
author_facet | Zheng, Yanfen Xu, Zongchang Liu, Haodong Liu, Yan Zhou, Yanan Meng, Chen Ma, Siqi Xie, Zhihong Li, Yiqiang Zhang, Cheng-Sheng |
author_sort | Zheng, Yanfen |
collection | PubMed |
description | Salinity is an important abiotic stress affecting plant growth. We have known that plants can recruit beneficial microbes from the surrounding soil. However, the ecological functions of the core microbiome in salt-tolerant plants, together with their driving factors, remain largely unexplored. Here, we employed both amplicon and shotgun metagenomic sequencing to investigate the microbiome and function signatures of bulk soil and rhizocompartment samples from three salt-tolerant plants (legumes Glycine soja and Sesbania cannabina and nonlegume Sorghum bicolor). Strong filtration effects for microbes and functional genes were found in the rhizocompartments following a spatial gradient. The dominant bacteria belonged to Ensifer for legumes and Bacillus for S. bicolor. Although different salt-tolerant plants harbored distinct bacterial communities, they all enriched genes involved in cell motility, Na(+) transport, and plant growth-promoting function (e.g., nitrogen fixation and phosphate solubilization) in rhizoplane soils, implying that the microbiome assembly of salt-tolerant plants might depend on the ecological functions of microbes rather than microbial taxa. Moreover, three metagenome-assembled genomes affiliated to Ensifer were obtained, and their genetic basis for salt stress alleviation were predicted. Soil pH, electrical conductivity, and total nitrogen were the most important driving factors for explaining the above microbial and functional gene selection. Correspondingly, the growth of an endophyte, Ensifer meliloti CL09, was enhanced by providing root exudates, suggesting that root exudates might be one of factors in the selection of rhizosphere and endosphere microbiota. Overall, this study reveals the ecological functions of the populations inhabiting the root of salt-tolerant plants. IMPORTANCE Salinity is an important but little-studied abiotic stressor affecting plant growth. Although several previous reports have examined salt-tolerant plant microbial communities, we still lack a comprehensive understanding about the functional characteristics and genomic information of this population. The results of this study revealed the root-enriched and -depleted bacterial groups, and found three salt-tolerant plants harbored different bacterial populations. The prediction of three metagenome-assembled genomes confirmed the critical role of root dominant species in helping plants tolerate salt stress. Further analysis indicated that plants enriched microbiome from soil according to their ecological functions but not microbial taxa. This highlights the importance of microbial function in enhancing plant adaptability to saline soil and implies that we should pay more attention to microbial function and not only to taxonomic information. Ultimately, these results provide insight for future agriculture using the various functions of microorganisms on the saline soil. |
format | Online Article Text |
id | pubmed-8549722 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-85497222021-11-08 Patterns in the Microbial Community of Salt-Tolerant Plants and the Functional Genes Associated with Salt Stress Alleviation Zheng, Yanfen Xu, Zongchang Liu, Haodong Liu, Yan Zhou, Yanan Meng, Chen Ma, Siqi Xie, Zhihong Li, Yiqiang Zhang, Cheng-Sheng Microbiol Spectr Research Article Salinity is an important abiotic stress affecting plant growth. We have known that plants can recruit beneficial microbes from the surrounding soil. However, the ecological functions of the core microbiome in salt-tolerant plants, together with their driving factors, remain largely unexplored. Here, we employed both amplicon and shotgun metagenomic sequencing to investigate the microbiome and function signatures of bulk soil and rhizocompartment samples from three salt-tolerant plants (legumes Glycine soja and Sesbania cannabina and nonlegume Sorghum bicolor). Strong filtration effects for microbes and functional genes were found in the rhizocompartments following a spatial gradient. The dominant bacteria belonged to Ensifer for legumes and Bacillus for S. bicolor. Although different salt-tolerant plants harbored distinct bacterial communities, they all enriched genes involved in cell motility, Na(+) transport, and plant growth-promoting function (e.g., nitrogen fixation and phosphate solubilization) in rhizoplane soils, implying that the microbiome assembly of salt-tolerant plants might depend on the ecological functions of microbes rather than microbial taxa. Moreover, three metagenome-assembled genomes affiliated to Ensifer were obtained, and their genetic basis for salt stress alleviation were predicted. Soil pH, electrical conductivity, and total nitrogen were the most important driving factors for explaining the above microbial and functional gene selection. Correspondingly, the growth of an endophyte, Ensifer meliloti CL09, was enhanced by providing root exudates, suggesting that root exudates might be one of factors in the selection of rhizosphere and endosphere microbiota. Overall, this study reveals the ecological functions of the populations inhabiting the root of salt-tolerant plants. IMPORTANCE Salinity is an important but little-studied abiotic stressor affecting plant growth. Although several previous reports have examined salt-tolerant plant microbial communities, we still lack a comprehensive understanding about the functional characteristics and genomic information of this population. The results of this study revealed the root-enriched and -depleted bacterial groups, and found three salt-tolerant plants harbored different bacterial populations. The prediction of three metagenome-assembled genomes confirmed the critical role of root dominant species in helping plants tolerate salt stress. Further analysis indicated that plants enriched microbiome from soil according to their ecological functions but not microbial taxa. This highlights the importance of microbial function in enhancing plant adaptability to saline soil and implies that we should pay more attention to microbial function and not only to taxonomic information. Ultimately, these results provide insight for future agriculture using the various functions of microorganisms on the saline soil. American Society for Microbiology 2021-10-27 /pmc/articles/PMC8549722/ /pubmed/34704793 http://dx.doi.org/10.1128/Spectrum.00767-21 Text en Copyright © 2021 Zheng et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Article Zheng, Yanfen Xu, Zongchang Liu, Haodong Liu, Yan Zhou, Yanan Meng, Chen Ma, Siqi Xie, Zhihong Li, Yiqiang Zhang, Cheng-Sheng Patterns in the Microbial Community of Salt-Tolerant Plants and the Functional Genes Associated with Salt Stress Alleviation |
title | Patterns in the Microbial Community of Salt-Tolerant Plants and the Functional Genes Associated with Salt Stress Alleviation |
title_full | Patterns in the Microbial Community of Salt-Tolerant Plants and the Functional Genes Associated with Salt Stress Alleviation |
title_fullStr | Patterns in the Microbial Community of Salt-Tolerant Plants and the Functional Genes Associated with Salt Stress Alleviation |
title_full_unstemmed | Patterns in the Microbial Community of Salt-Tolerant Plants and the Functional Genes Associated with Salt Stress Alleviation |
title_short | Patterns in the Microbial Community of Salt-Tolerant Plants and the Functional Genes Associated with Salt Stress Alleviation |
title_sort | patterns in the microbial community of salt-tolerant plants and the functional genes associated with salt stress alleviation |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8549722/ https://www.ncbi.nlm.nih.gov/pubmed/34704793 http://dx.doi.org/10.1128/Spectrum.00767-21 |
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