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Different dynamics of genome content shuffling among host-specificity groups of the symbiotic actinobacterium Frankia
BACKGROUND: Frankia is a genus of soil actinobacteria forming nitrogen-fixing root-nodule symbiotic relationships with non-leguminous woody plant species, collectively called actinorhizals, from eight dicotyledonous families. Frankia strains are classified into four host-specificity groups (HSGs), e...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2014
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4117964/ https://www.ncbi.nlm.nih.gov/pubmed/25038796 http://dx.doi.org/10.1186/1471-2164-15-609 |
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author | Kucho, Ken-ichi Yamanaka, Takashi Sasakawa, Hideo Mansour, Samira R Uchiumi, Toshiki |
author_facet | Kucho, Ken-ichi Yamanaka, Takashi Sasakawa, Hideo Mansour, Samira R Uchiumi, Toshiki |
author_sort | Kucho, Ken-ichi |
collection | PubMed |
description | BACKGROUND: Frankia is a genus of soil actinobacteria forming nitrogen-fixing root-nodule symbiotic relationships with non-leguminous woody plant species, collectively called actinorhizals, from eight dicotyledonous families. Frankia strains are classified into four host-specificity groups (HSGs), each of which exhibits a distinct host range. Genome sizes of representative strains of Alnus, Casuarina, and Elaeagnus HSGs are highly diverged and are positively correlated with the size of their host ranges. RESULTS: The content and size of 12 Frankia genomes were investigated by in silico comparative genome hybridization and pulsed-field gel electrophoresis, respectively. Data were collected from four query strains of each HSG and compared with those of reference strains possessing completely sequenced genomes. The degree of difference in genome content between query and reference strains varied depending on HSG. Elaeagnus query strains were missing the greatest number (22–32%) of genes compared with the corresponding reference genome; Casuarina query strains lacked the fewest (0–4%), with Alnus query strains intermediate (14–18%). In spite of the remarkable gene loss, genome sizes of Alnus and Elaeagnus query strains were larger than would be expected based on total length of the absent genes. In contrast, Casuarina query strains had smaller genomes than expected. CONCLUSIONS: The positive correlation between genome size and host range held true across all investigated strains, supporting the hypothesis that size and genome content differences are responsible for observed diversity in host plants and host plant biogeography among Frankia strains. In addition, our results suggest that different dynamics of shuffling of genome content have contributed to these symbiotic and biogeographic adaptations. Elaeagnus strains, and to a lesser extent Alnus strains, have gained and lost many genes to adapt to a wide range of environments and host plants. Conversely, rather than acquiring new genes, Casuarina strains have discarded genes to reduce genome size, suggesting an evolutionary orientation towards existence as specialist symbionts. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-609) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-4117964 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2014 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-41179642014-08-05 Different dynamics of genome content shuffling among host-specificity groups of the symbiotic actinobacterium Frankia Kucho, Ken-ichi Yamanaka, Takashi Sasakawa, Hideo Mansour, Samira R Uchiumi, Toshiki BMC Genomics Research Article BACKGROUND: Frankia is a genus of soil actinobacteria forming nitrogen-fixing root-nodule symbiotic relationships with non-leguminous woody plant species, collectively called actinorhizals, from eight dicotyledonous families. Frankia strains are classified into four host-specificity groups (HSGs), each of which exhibits a distinct host range. Genome sizes of representative strains of Alnus, Casuarina, and Elaeagnus HSGs are highly diverged and are positively correlated with the size of their host ranges. RESULTS: The content and size of 12 Frankia genomes were investigated by in silico comparative genome hybridization and pulsed-field gel electrophoresis, respectively. Data were collected from four query strains of each HSG and compared with those of reference strains possessing completely sequenced genomes. The degree of difference in genome content between query and reference strains varied depending on HSG. Elaeagnus query strains were missing the greatest number (22–32%) of genes compared with the corresponding reference genome; Casuarina query strains lacked the fewest (0–4%), with Alnus query strains intermediate (14–18%). In spite of the remarkable gene loss, genome sizes of Alnus and Elaeagnus query strains were larger than would be expected based on total length of the absent genes. In contrast, Casuarina query strains had smaller genomes than expected. CONCLUSIONS: The positive correlation between genome size and host range held true across all investigated strains, supporting the hypothesis that size and genome content differences are responsible for observed diversity in host plants and host plant biogeography among Frankia strains. In addition, our results suggest that different dynamics of shuffling of genome content have contributed to these symbiotic and biogeographic adaptations. Elaeagnus strains, and to a lesser extent Alnus strains, have gained and lost many genes to adapt to a wide range of environments and host plants. Conversely, rather than acquiring new genes, Casuarina strains have discarded genes to reduce genome size, suggesting an evolutionary orientation towards existence as specialist symbionts. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-609) contains supplementary material, which is available to authorized users. BioMed Central 2014-07-19 /pmc/articles/PMC4117964/ /pubmed/25038796 http://dx.doi.org/10.1186/1471-2164-15-609 Text en © Kucho et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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 Kucho, Ken-ichi Yamanaka, Takashi Sasakawa, Hideo Mansour, Samira R Uchiumi, Toshiki Different dynamics of genome content shuffling among host-specificity groups of the symbiotic actinobacterium Frankia |
title | Different dynamics of genome content shuffling among host-specificity groups of the symbiotic actinobacterium Frankia |
title_full | Different dynamics of genome content shuffling among host-specificity groups of the symbiotic actinobacterium Frankia |
title_fullStr | Different dynamics of genome content shuffling among host-specificity groups of the symbiotic actinobacterium Frankia |
title_full_unstemmed | Different dynamics of genome content shuffling among host-specificity groups of the symbiotic actinobacterium Frankia |
title_short | Different dynamics of genome content shuffling among host-specificity groups of the symbiotic actinobacterium Frankia |
title_sort | different dynamics of genome content shuffling among host-specificity groups of the symbiotic actinobacterium frankia |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4117964/ https://www.ncbi.nlm.nih.gov/pubmed/25038796 http://dx.doi.org/10.1186/1471-2164-15-609 |
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