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A microorganisms’ journey between plant generations

BACKGROUND: Plants are colonized by a great diversity of microorganisms which form a microbiota and perform additional functions for their host. This microbiota can thus be considered a toolbox enabling plants to buffer local environmental changes, with a positive influence on plant fitness. In this...

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Autores principales: Vannier, Nathan, Mony, Cendrine, Bittebiere, Anne-Kristel, Michon-Coudouel, Sophie, Biget, Marine, Vandenkoornhuyse, Philippe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5918900/
https://www.ncbi.nlm.nih.gov/pubmed/29695286
http://dx.doi.org/10.1186/s40168-018-0459-7
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author Vannier, Nathan
Mony, Cendrine
Bittebiere, Anne-Kristel
Michon-Coudouel, Sophie
Biget, Marine
Vandenkoornhuyse, Philippe
author_facet Vannier, Nathan
Mony, Cendrine
Bittebiere, Anne-Kristel
Michon-Coudouel, Sophie
Biget, Marine
Vandenkoornhuyse, Philippe
author_sort Vannier, Nathan
collection PubMed
description BACKGROUND: Plants are colonized by a great diversity of microorganisms which form a microbiota and perform additional functions for their host. This microbiota can thus be considered a toolbox enabling plants to buffer local environmental changes, with a positive influence on plant fitness. In this context, the transmission of the microbiota to the progeny represent a way to ensure the presence of beneficial symbionts within the habitat. Examples of such transmission have been mainly described for seed transmission and concern a few pathogenic microorganisms. We investigated the transmission of symbiotic partners to plant progeny within clonal plant network. METHODS: We used the clonal plant Glechoma hederacea as plant model and forced newly emitted clonal progeny to root in separated pots while controlling the presence of microorganisms. We used an amplicon sequencing approach of 16S and 18S rRNA targeting bacteria/archaea and fungi respectively to describe the root microbiota of mother and clonal-plant offspring. RESULTS: We demonstrated the vertical transmission of a significant proportion of the mother plants’ symbiotic bacteria and fungi to the daughters. Interestingly, archaea were not transmitted to the daughter plants. Transmitted communities had lower richness, suggesting a filtration during transmission. We found that the transmitted pool of microorganisms was similar among daughters, constituting the heritability of a specific cohort of microorganisms, opening a new understanding of the plant holobiont. We also found significant effects of distance to the mother plant and of growth time on the richness of the microbiota transmitted. CONCLUSIONS: In this clonal plant, microorganisms are transmitted between individuals through connections, thereby ensuring the availability of microbe partners for the newborn plants as well as the dispersion between hosts for the microorganisms. This previously undescribed ecological process allows the dispersal of microorganisms in space and across plant generations. As the vast majority of plants are clonal, this process might be therefore a strong driver of ecosystem functioning and assembly of plant and microorganism communities in a wide range of ecosystems. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0459-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-59189002018-04-30 A microorganisms’ journey between plant generations Vannier, Nathan Mony, Cendrine Bittebiere, Anne-Kristel Michon-Coudouel, Sophie Biget, Marine Vandenkoornhuyse, Philippe Microbiome Research BACKGROUND: Plants are colonized by a great diversity of microorganisms which form a microbiota and perform additional functions for their host. This microbiota can thus be considered a toolbox enabling plants to buffer local environmental changes, with a positive influence on plant fitness. In this context, the transmission of the microbiota to the progeny represent a way to ensure the presence of beneficial symbionts within the habitat. Examples of such transmission have been mainly described for seed transmission and concern a few pathogenic microorganisms. We investigated the transmission of symbiotic partners to plant progeny within clonal plant network. METHODS: We used the clonal plant Glechoma hederacea as plant model and forced newly emitted clonal progeny to root in separated pots while controlling the presence of microorganisms. We used an amplicon sequencing approach of 16S and 18S rRNA targeting bacteria/archaea and fungi respectively to describe the root microbiota of mother and clonal-plant offspring. RESULTS: We demonstrated the vertical transmission of a significant proportion of the mother plants’ symbiotic bacteria and fungi to the daughters. Interestingly, archaea were not transmitted to the daughter plants. Transmitted communities had lower richness, suggesting a filtration during transmission. We found that the transmitted pool of microorganisms was similar among daughters, constituting the heritability of a specific cohort of microorganisms, opening a new understanding of the plant holobiont. We also found significant effects of distance to the mother plant and of growth time on the richness of the microbiota transmitted. CONCLUSIONS: In this clonal plant, microorganisms are transmitted between individuals through connections, thereby ensuring the availability of microbe partners for the newborn plants as well as the dispersion between hosts for the microorganisms. This previously undescribed ecological process allows the dispersal of microorganisms in space and across plant generations. As the vast majority of plants are clonal, this process might be therefore a strong driver of ecosystem functioning and assembly of plant and microorganism communities in a wide range of ecosystems. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0459-7) contains supplementary material, which is available to authorized users. BioMed Central 2018-04-26 /pmc/articles/PMC5918900/ /pubmed/29695286 http://dx.doi.org/10.1186/s40168-018-0459-7 Text en © The Author(s). 2018 Open Access This 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
Vannier, Nathan
Mony, Cendrine
Bittebiere, Anne-Kristel
Michon-Coudouel, Sophie
Biget, Marine
Vandenkoornhuyse, Philippe
A microorganisms’ journey between plant generations
title A microorganisms’ journey between plant generations
title_full A microorganisms’ journey between plant generations
title_fullStr A microorganisms’ journey between plant generations
title_full_unstemmed A microorganisms’ journey between plant generations
title_short A microorganisms’ journey between plant generations
title_sort microorganisms’ journey between plant generations
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5918900/
https://www.ncbi.nlm.nih.gov/pubmed/29695286
http://dx.doi.org/10.1186/s40168-018-0459-7
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