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Genomic insight into the origins and evolution of symbiosis genes in Phaseolus vulgaris microsymbionts
BACKGROUND: Phaseolus vulgaris (common bean) microsymbionts belonging to the bacterial genera Rhizobium, Bradyrhizobium, and Ensifer (Sinorhizobium) have been isolated across the globe. Individual symbiosis genes (e.g., nodC) of these rhizobia can be different within each genus and among distinct ge...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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BioMed Central
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7047383/ https://www.ncbi.nlm.nih.gov/pubmed/32106817 http://dx.doi.org/10.1186/s12864-020-6578-0 |
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author | Tong, Wenjun Li, Xiangchen Wang, Entao Cao, Ying Chen, Weimin Tao, Shiheng Wei, Gehong |
author_facet | Tong, Wenjun Li, Xiangchen Wang, Entao Cao, Ying Chen, Weimin Tao, Shiheng Wei, Gehong |
author_sort | Tong, Wenjun |
collection | PubMed |
description | BACKGROUND: Phaseolus vulgaris (common bean) microsymbionts belonging to the bacterial genera Rhizobium, Bradyrhizobium, and Ensifer (Sinorhizobium) have been isolated across the globe. Individual symbiosis genes (e.g., nodC) of these rhizobia can be different within each genus and among distinct genera. Little information is available about the symbiotic structure of indigenous Rhizobium strains nodulating introduced bean plants or the emergence of a symbiotic ability to associate with bean plants in Bradyrhizobium and Ensifer strains. Here, we sequenced the genomes of 29 representative bean microsymbionts (21 Rhizobium, four Ensifer, and four Bradyrhizobium) and compared them with closely related reference strains to estimate the origins of symbiosis genes among these Chinese bean microsymbionts. RESULTS: Comparative genomics demonstrated horizontal gene transfer exclusively at the plasmid level, leading to expanded diversity of bean-nodulating Rhizobium strains. Analysis of vertically transferred genes uncovered 191 (out of the 2654) single-copy core genes with phylogenies strictly consistent with the taxonomic status of bacterial species, but none were found on symbiosis plasmids. A common symbiotic region was wholly conserved within the Rhizobium genus yet different from those of the other two genera. A single strain of Ensifer and two Bradyrhizobium strains shared similar gene content with soybean microsymbionts in both chromosomes and symbiotic regions. CONCLUSIONS: The 19 native bean Rhizobium microsymbionts were assigned to four defined species and six putative novel species. The symbiosis genes of R. phaseoli, R. sophoriradicis, and R. esperanzae strains that originated from Mexican bean-nodulating strains were possibly introduced alongside bean seeds. R. anhuiense strains displayed distinct host ranges, indicating transition into bean microsymbionts. Among the six putative novel species exclusive to China, horizontal transfer of symbiosis genes suggested symbiosis with other indigenous legumes and loss of originally symbiotic regions or non-symbionts before the introduction of common bean into China. Genome data for Ensifer and Bradyrhizobium strains indicated symbiotic compatibility between microsymbionts of common bean and other hosts such as soybean. |
format | Online Article Text |
id | pubmed-7047383 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-70473832020-03-03 Genomic insight into the origins and evolution of symbiosis genes in Phaseolus vulgaris microsymbionts Tong, Wenjun Li, Xiangchen Wang, Entao Cao, Ying Chen, Weimin Tao, Shiheng Wei, Gehong BMC Genomics Research Article BACKGROUND: Phaseolus vulgaris (common bean) microsymbionts belonging to the bacterial genera Rhizobium, Bradyrhizobium, and Ensifer (Sinorhizobium) have been isolated across the globe. Individual symbiosis genes (e.g., nodC) of these rhizobia can be different within each genus and among distinct genera. Little information is available about the symbiotic structure of indigenous Rhizobium strains nodulating introduced bean plants or the emergence of a symbiotic ability to associate with bean plants in Bradyrhizobium and Ensifer strains. Here, we sequenced the genomes of 29 representative bean microsymbionts (21 Rhizobium, four Ensifer, and four Bradyrhizobium) and compared them with closely related reference strains to estimate the origins of symbiosis genes among these Chinese bean microsymbionts. RESULTS: Comparative genomics demonstrated horizontal gene transfer exclusively at the plasmid level, leading to expanded diversity of bean-nodulating Rhizobium strains. Analysis of vertically transferred genes uncovered 191 (out of the 2654) single-copy core genes with phylogenies strictly consistent with the taxonomic status of bacterial species, but none were found on symbiosis plasmids. A common symbiotic region was wholly conserved within the Rhizobium genus yet different from those of the other two genera. A single strain of Ensifer and two Bradyrhizobium strains shared similar gene content with soybean microsymbionts in both chromosomes and symbiotic regions. CONCLUSIONS: The 19 native bean Rhizobium microsymbionts were assigned to four defined species and six putative novel species. The symbiosis genes of R. phaseoli, R. sophoriradicis, and R. esperanzae strains that originated from Mexican bean-nodulating strains were possibly introduced alongside bean seeds. R. anhuiense strains displayed distinct host ranges, indicating transition into bean microsymbionts. Among the six putative novel species exclusive to China, horizontal transfer of symbiosis genes suggested symbiosis with other indigenous legumes and loss of originally symbiotic regions or non-symbionts before the introduction of common bean into China. Genome data for Ensifer and Bradyrhizobium strains indicated symbiotic compatibility between microsymbionts of common bean and other hosts such as soybean. BioMed Central 2020-02-27 /pmc/articles/PMC7047383/ /pubmed/32106817 http://dx.doi.org/10.1186/s12864-020-6578-0 Text en © The Author(s). 2020 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Article Tong, Wenjun Li, Xiangchen Wang, Entao Cao, Ying Chen, Weimin Tao, Shiheng Wei, Gehong Genomic insight into the origins and evolution of symbiosis genes in Phaseolus vulgaris microsymbionts |
title | Genomic insight into the origins and evolution of symbiosis genes in Phaseolus vulgaris microsymbionts |
title_full | Genomic insight into the origins and evolution of symbiosis genes in Phaseolus vulgaris microsymbionts |
title_fullStr | Genomic insight into the origins and evolution of symbiosis genes in Phaseolus vulgaris microsymbionts |
title_full_unstemmed | Genomic insight into the origins and evolution of symbiosis genes in Phaseolus vulgaris microsymbionts |
title_short | Genomic insight into the origins and evolution of symbiosis genes in Phaseolus vulgaris microsymbionts |
title_sort | genomic insight into the origins and evolution of symbiosis genes in phaseolus vulgaris microsymbionts |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7047383/ https://www.ncbi.nlm.nih.gov/pubmed/32106817 http://dx.doi.org/10.1186/s12864-020-6578-0 |
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