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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,...

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Autores principales: Zheng, Yanfen, Xu, Zongchang, Liu, Haodong, Liu, Yan, Zhou, Yanan, Meng, Chen, Ma, Siqi, Xie, Zhihong, Li, Yiqiang, Zhang, Cheng-Sheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
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.
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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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