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Mycorrhizae Enhance Soybean Plant Growth and Aluminum Stress Tolerance by Shaping the Microbiome Assembly in an Acidic Soil
Strongly acidic soils are characterized by high aluminum (Al) toxicity and low phosphorus (P) availability, which suppress legume plant growth and nodule development. Arbuscular mycorrhizal fungi (AMF) stimulate rhizobia and enhance plant P uptake. However, it is unclear how this symbiotic soybean-A...
Autores principales: | , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10100836/ https://www.ncbi.nlm.nih.gov/pubmed/36916950 http://dx.doi.org/10.1128/spectrum.03310-22 |
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author | Wen, Zhongling Yang, Minkai Han, Hongwei Fazal, Aliya Liao, Yonghui Ren, Ran Yin, Tongming Qi, Jinliang Sun, Shucun Lu, Guihua Hu, Shuijin Yang, Yonghua |
author_facet | Wen, Zhongling Yang, Minkai Han, Hongwei Fazal, Aliya Liao, Yonghui Ren, Ran Yin, Tongming Qi, Jinliang Sun, Shucun Lu, Guihua Hu, Shuijin Yang, Yonghua |
author_sort | Wen, Zhongling |
collection | PubMed |
description | Strongly acidic soils are characterized by high aluminum (Al) toxicity and low phosphorus (P) availability, which suppress legume plant growth and nodule development. Arbuscular mycorrhizal fungi (AMF) stimulate rhizobia and enhance plant P uptake. However, it is unclear how this symbiotic soybean-AMF-rhizobial trio promotes soybean growth in acidic soils. We examined the effects of AMF and rhizobium addition on the growth of two soybean genotypes, namely, Al-tolerant and Al-sensitive soybeans as well as their associated bacterial and fungal communities in an acidic soil. With and without rhizobial addition, AMF significantly increased the fresh shoot and root biomass of Al-tolerant soybean by 47%/87% and 37%/24%, respectively. This increase in plant biomass corresponded to the enrichment of four plant growth-promoting rhizobacteria (PGPR) in the rhizospheric soil, namely, Chitinophagaceae bacterium 4GSH07, Paraburkholderia soli, Sinomonas atrocyanea, and Aquincola tertiaricarbonis. For Al-sensitive soybean, AMF addition increased the fresh shoot and root biomass by 112%/64% and 30%/217%, respectively, with/without rhizobial addition. Interestingly, this significant increase coincided with a decrease in the pathogenic fungus Nigrospora oryzae as well as an increase in S. atrocyanea, A. tertiaricarbonis, and Talaromyces verruculosus (a P-solubilizing fungus) in the rhizospheric soil. Lastly, the compartment niche along the soil-plant continuum shaped microbiome assembly, with pathogenic/saprotrophic microbes accumulating in the rhizospheric soil and PGPR related to nitrogen fixation or stress resistance (e.g., Rhizobium leguminosarum and Sphingomonas azotifigens) accumulating in the endospheric layer. IMPORTANCE Taken together, this study examined the effects of arbuscular mycorrhizal fungi (AMF) and rhizobial combinations on the growth of Al-tolerant and Al-sensitive soybeans as well as their associated microbial communities in acidic soils and concluded that AMF enhances soybean growth and Al stress tolerance by recruiting PGPR and altering the root-associated microbiome assembly in a host-dependent manner. In the future, these findings will help us better understand the impacts of AMF on rhizosphere microbiome assembly and will contribute to the development of soybean breeding techniques for the comprehensive use of PGPR in sustainable agriculture. |
format | Online Article Text |
id | pubmed-10100836 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-101008362023-04-14 Mycorrhizae Enhance Soybean Plant Growth and Aluminum Stress Tolerance by Shaping the Microbiome Assembly in an Acidic Soil Wen, Zhongling Yang, Minkai Han, Hongwei Fazal, Aliya Liao, Yonghui Ren, Ran Yin, Tongming Qi, Jinliang Sun, Shucun Lu, Guihua Hu, Shuijin Yang, Yonghua Microbiol Spectr Research Article Strongly acidic soils are characterized by high aluminum (Al) toxicity and low phosphorus (P) availability, which suppress legume plant growth and nodule development. Arbuscular mycorrhizal fungi (AMF) stimulate rhizobia and enhance plant P uptake. However, it is unclear how this symbiotic soybean-AMF-rhizobial trio promotes soybean growth in acidic soils. We examined the effects of AMF and rhizobium addition on the growth of two soybean genotypes, namely, Al-tolerant and Al-sensitive soybeans as well as their associated bacterial and fungal communities in an acidic soil. With and without rhizobial addition, AMF significantly increased the fresh shoot and root biomass of Al-tolerant soybean by 47%/87% and 37%/24%, respectively. This increase in plant biomass corresponded to the enrichment of four plant growth-promoting rhizobacteria (PGPR) in the rhizospheric soil, namely, Chitinophagaceae bacterium 4GSH07, Paraburkholderia soli, Sinomonas atrocyanea, and Aquincola tertiaricarbonis. For Al-sensitive soybean, AMF addition increased the fresh shoot and root biomass by 112%/64% and 30%/217%, respectively, with/without rhizobial addition. Interestingly, this significant increase coincided with a decrease in the pathogenic fungus Nigrospora oryzae as well as an increase in S. atrocyanea, A. tertiaricarbonis, and Talaromyces verruculosus (a P-solubilizing fungus) in the rhizospheric soil. Lastly, the compartment niche along the soil-plant continuum shaped microbiome assembly, with pathogenic/saprotrophic microbes accumulating in the rhizospheric soil and PGPR related to nitrogen fixation or stress resistance (e.g., Rhizobium leguminosarum and Sphingomonas azotifigens) accumulating in the endospheric layer. IMPORTANCE Taken together, this study examined the effects of arbuscular mycorrhizal fungi (AMF) and rhizobial combinations on the growth of Al-tolerant and Al-sensitive soybeans as well as their associated microbial communities in acidic soils and concluded that AMF enhances soybean growth and Al stress tolerance by recruiting PGPR and altering the root-associated microbiome assembly in a host-dependent manner. In the future, these findings will help us better understand the impacts of AMF on rhizosphere microbiome assembly and will contribute to the development of soybean breeding techniques for the comprehensive use of PGPR in sustainable agriculture. American Society for Microbiology 2023-03-14 /pmc/articles/PMC10100836/ /pubmed/36916950 http://dx.doi.org/10.1128/spectrum.03310-22 Text en Copyright © 2023 Wen 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 Wen, Zhongling Yang, Minkai Han, Hongwei Fazal, Aliya Liao, Yonghui Ren, Ran Yin, Tongming Qi, Jinliang Sun, Shucun Lu, Guihua Hu, Shuijin Yang, Yonghua Mycorrhizae Enhance Soybean Plant Growth and Aluminum Stress Tolerance by Shaping the Microbiome Assembly in an Acidic Soil |
title | Mycorrhizae Enhance Soybean Plant Growth and Aluminum Stress Tolerance by Shaping the Microbiome Assembly in an Acidic Soil |
title_full | Mycorrhizae Enhance Soybean Plant Growth and Aluminum Stress Tolerance by Shaping the Microbiome Assembly in an Acidic Soil |
title_fullStr | Mycorrhizae Enhance Soybean Plant Growth and Aluminum Stress Tolerance by Shaping the Microbiome Assembly in an Acidic Soil |
title_full_unstemmed | Mycorrhizae Enhance Soybean Plant Growth and Aluminum Stress Tolerance by Shaping the Microbiome Assembly in an Acidic Soil |
title_short | Mycorrhizae Enhance Soybean Plant Growth and Aluminum Stress Tolerance by Shaping the Microbiome Assembly in an Acidic Soil |
title_sort | mycorrhizae enhance soybean plant growth and aluminum stress tolerance by shaping the microbiome assembly in an acidic soil |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10100836/ https://www.ncbi.nlm.nih.gov/pubmed/36916950 http://dx.doi.org/10.1128/spectrum.03310-22 |
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