Cargando…

A genetically and functionally diverse group of non-diazotrophic Bradyrhizobium spp. colonizes the root endophytic compartment of Arabidopsis thaliana

BACKGROUND: Diazotrophic Bradyrhizobium spp. are well known for their ability to trigger nodule formation on a variety of legume species. In nodules, Bradyrhizobium utilizes plant-derived carbohydrates in exchange for fixed nitrogen. The genes essential for the nodulation and nitrogen-fixation trait...

Descripción completa

Detalles Bibliográficos
Autores principales: Schneijderberg, Martinus, Schmitz, Lucas, Cheng, Xu, Polman, Sharon, Franken, Carolien, Geurts, Rene, Bisseling, Ton
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5896095/
https://www.ncbi.nlm.nih.gov/pubmed/29642886
http://dx.doi.org/10.1186/s12870-018-1272-y
_version_ 1783313773936771072
author Schneijderberg, Martinus
Schmitz, Lucas
Cheng, Xu
Polman, Sharon
Franken, Carolien
Geurts, Rene
Bisseling, Ton
author_facet Schneijderberg, Martinus
Schmitz, Lucas
Cheng, Xu
Polman, Sharon
Franken, Carolien
Geurts, Rene
Bisseling, Ton
author_sort Schneijderberg, Martinus
collection PubMed
description BACKGROUND: Diazotrophic Bradyrhizobium spp. are well known for their ability to trigger nodule formation on a variety of legume species. In nodules, Bradyrhizobium utilizes plant-derived carbohydrates in exchange for fixed nitrogen. The genes essential for the nodulation and nitrogen-fixation trait are clustered in a genomic region, which is known as the ‘symbiotic island’. Recently, novel non-diazotrophic Bradyrhizobium spp. have been found to be highly abundant in soils, suggesting that these species can also have a ‘free-living’ life history. However, whether non-diazotrophic Bradyrhizobium spp. can live in association with plants remains elusive. RESULTS: In this study, we show that Bradyrhizobium spp. are common root endophytes of non-legume plant species – including Arabidopsis thaliana (Arabidopsis) – grown in an ecological setting. From a single Arabidopsis root, four Bradyrhizobium sp. strains (designated MOS001 to MOS004) were isolated. Comparative genome analysis revealed that these strains were genetically and functionally highly diverse, but did not harbour the nodulation and the nitrogen fixation gene clusters. Comparative colonization experiments, with MOS strains and nitrogen-fixing symbiotic strains, revealed that all tested Bradyrhizobium spp. can colonize the root endophytic compartment of Arabidopsis. CONCLUSION: This study provides evidence that both diazotrophic and non-diazotrophic Bradyrhizobium spp. colonize the root endophytic compartment of a wide variety of plant species, including the model species Arabidopsis. This demonstrates that plant roots form a major ecological niche for Bradyrhizobium spp., which might be ancestral to the evolution of the nodulation and nitrogen-fixation trait in this genus. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-018-1272-y) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-5896095
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-58960952018-04-20 A genetically and functionally diverse group of non-diazotrophic Bradyrhizobium spp. colonizes the root endophytic compartment of Arabidopsis thaliana Schneijderberg, Martinus Schmitz, Lucas Cheng, Xu Polman, Sharon Franken, Carolien Geurts, Rene Bisseling, Ton BMC Plant Biol Research Article BACKGROUND: Diazotrophic Bradyrhizobium spp. are well known for their ability to trigger nodule formation on a variety of legume species. In nodules, Bradyrhizobium utilizes plant-derived carbohydrates in exchange for fixed nitrogen. The genes essential for the nodulation and nitrogen-fixation trait are clustered in a genomic region, which is known as the ‘symbiotic island’. Recently, novel non-diazotrophic Bradyrhizobium spp. have been found to be highly abundant in soils, suggesting that these species can also have a ‘free-living’ life history. However, whether non-diazotrophic Bradyrhizobium spp. can live in association with plants remains elusive. RESULTS: In this study, we show that Bradyrhizobium spp. are common root endophytes of non-legume plant species – including Arabidopsis thaliana (Arabidopsis) – grown in an ecological setting. From a single Arabidopsis root, four Bradyrhizobium sp. strains (designated MOS001 to MOS004) were isolated. Comparative genome analysis revealed that these strains were genetically and functionally highly diverse, but did not harbour the nodulation and the nitrogen fixation gene clusters. Comparative colonization experiments, with MOS strains and nitrogen-fixing symbiotic strains, revealed that all tested Bradyrhizobium spp. can colonize the root endophytic compartment of Arabidopsis. CONCLUSION: This study provides evidence that both diazotrophic and non-diazotrophic Bradyrhizobium spp. colonize the root endophytic compartment of a wide variety of plant species, including the model species Arabidopsis. This demonstrates that plant roots form a major ecological niche for Bradyrhizobium spp., which might be ancestral to the evolution of the nodulation and nitrogen-fixation trait in this genus. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-018-1272-y) contains supplementary material, which is available to authorized users. BioMed Central 2018-04-11 /pmc/articles/PMC5896095/ /pubmed/29642886 http://dx.doi.org/10.1186/s12870-018-1272-y Text en © The Author(s). 2018 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
Schneijderberg, Martinus
Schmitz, Lucas
Cheng, Xu
Polman, Sharon
Franken, Carolien
Geurts, Rene
Bisseling, Ton
A genetically and functionally diverse group of non-diazotrophic Bradyrhizobium spp. colonizes the root endophytic compartment of Arabidopsis thaliana
title A genetically and functionally diverse group of non-diazotrophic Bradyrhizobium spp. colonizes the root endophytic compartment of Arabidopsis thaliana
title_full A genetically and functionally diverse group of non-diazotrophic Bradyrhizobium spp. colonizes the root endophytic compartment of Arabidopsis thaliana
title_fullStr A genetically and functionally diverse group of non-diazotrophic Bradyrhizobium spp. colonizes the root endophytic compartment of Arabidopsis thaliana
title_full_unstemmed A genetically and functionally diverse group of non-diazotrophic Bradyrhizobium spp. colonizes the root endophytic compartment of Arabidopsis thaliana
title_short A genetically and functionally diverse group of non-diazotrophic Bradyrhizobium spp. colonizes the root endophytic compartment of Arabidopsis thaliana
title_sort genetically and functionally diverse group of non-diazotrophic bradyrhizobium spp. colonizes the root endophytic compartment of arabidopsis thaliana
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5896095/
https://www.ncbi.nlm.nih.gov/pubmed/29642886
http://dx.doi.org/10.1186/s12870-018-1272-y
work_keys_str_mv AT schneijderbergmartinus ageneticallyandfunctionallydiversegroupofnondiazotrophicbradyrhizobiumsppcolonizestherootendophyticcompartmentofarabidopsisthaliana
AT schmitzlucas ageneticallyandfunctionallydiversegroupofnondiazotrophicbradyrhizobiumsppcolonizestherootendophyticcompartmentofarabidopsisthaliana
AT chengxu ageneticallyandfunctionallydiversegroupofnondiazotrophicbradyrhizobiumsppcolonizestherootendophyticcompartmentofarabidopsisthaliana
AT polmansharon ageneticallyandfunctionallydiversegroupofnondiazotrophicbradyrhizobiumsppcolonizestherootendophyticcompartmentofarabidopsisthaliana
AT frankencarolien ageneticallyandfunctionallydiversegroupofnondiazotrophicbradyrhizobiumsppcolonizestherootendophyticcompartmentofarabidopsisthaliana
AT geurtsrene ageneticallyandfunctionallydiversegroupofnondiazotrophicbradyrhizobiumsppcolonizestherootendophyticcompartmentofarabidopsisthaliana
AT bisselington ageneticallyandfunctionallydiversegroupofnondiazotrophicbradyrhizobiumsppcolonizestherootendophyticcompartmentofarabidopsisthaliana
AT schneijderbergmartinus geneticallyandfunctionallydiversegroupofnondiazotrophicbradyrhizobiumsppcolonizestherootendophyticcompartmentofarabidopsisthaliana
AT schmitzlucas geneticallyandfunctionallydiversegroupofnondiazotrophicbradyrhizobiumsppcolonizestherootendophyticcompartmentofarabidopsisthaliana
AT chengxu geneticallyandfunctionallydiversegroupofnondiazotrophicbradyrhizobiumsppcolonizestherootendophyticcompartmentofarabidopsisthaliana
AT polmansharon geneticallyandfunctionallydiversegroupofnondiazotrophicbradyrhizobiumsppcolonizestherootendophyticcompartmentofarabidopsisthaliana
AT frankencarolien geneticallyandfunctionallydiversegroupofnondiazotrophicbradyrhizobiumsppcolonizestherootendophyticcompartmentofarabidopsisthaliana
AT geurtsrene geneticallyandfunctionallydiversegroupofnondiazotrophicbradyrhizobiumsppcolonizestherootendophyticcompartmentofarabidopsisthaliana
AT bisselington geneticallyandfunctionallydiversegroupofnondiazotrophicbradyrhizobiumsppcolonizestherootendophyticcompartmentofarabidopsisthaliana