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Co‐evolution within the plant holobiont drives host performance

Plants interact with a diversity of microorganisms that influence their growth and resilience, and they can therefore be considered as ecological entities, namely “plant holobionts,” rather than as singular organisms. In a plant holobiont, the assembly of above‐ and belowground microbiota is ruled b...

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Autores principales: Mesny, Fantin, Hacquard, Stéphane, Thomma, Bart PHJ
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10481671/
https://www.ncbi.nlm.nih.gov/pubmed/37471099
http://dx.doi.org/10.15252/embr.202357455
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author Mesny, Fantin
Hacquard, Stéphane
Thomma, Bart PHJ
author_facet Mesny, Fantin
Hacquard, Stéphane
Thomma, Bart PHJ
author_sort Mesny, Fantin
collection PubMed
description Plants interact with a diversity of microorganisms that influence their growth and resilience, and they can therefore be considered as ecological entities, namely “plant holobionts,” rather than as singular organisms. In a plant holobiont, the assembly of above‐ and belowground microbiota is ruled by host, microbial, and environmental factors. Upon microorganism perception, plants activate immune signaling resulting in the secretion of factors that modulate microbiota composition. Additionally, metabolic interdependencies and antagonism between microbes are driving forces for community assemblies. We argue that complex plant–microbe and intermicrobial interactions have been selected for during evolution and may promote the survival and fitness of plants and their associated microorganisms as holobionts. As part of this process, plants evolved metabolite‐mediated strategies to selectively recruit beneficial microorganisms in their microbiota. Some of these microbiota members show host‐adaptation, from which mutualism may rapidly arise. In the holobiont, microbiota members also co‐evolved antagonistic activities that restrict proliferation of microbes with high pathogenic potential and can therefore prevent disease development. Co‐evolution within holobionts thus ultimately drives plant performance.
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spelling pubmed-104816712023-09-07 Co‐evolution within the plant holobiont drives host performance Mesny, Fantin Hacquard, Stéphane Thomma, Bart PHJ EMBO Rep Reviews Plants interact with a diversity of microorganisms that influence their growth and resilience, and they can therefore be considered as ecological entities, namely “plant holobionts,” rather than as singular organisms. In a plant holobiont, the assembly of above‐ and belowground microbiota is ruled by host, microbial, and environmental factors. Upon microorganism perception, plants activate immune signaling resulting in the secretion of factors that modulate microbiota composition. Additionally, metabolic interdependencies and antagonism between microbes are driving forces for community assemblies. We argue that complex plant–microbe and intermicrobial interactions have been selected for during evolution and may promote the survival and fitness of plants and their associated microorganisms as holobionts. As part of this process, plants evolved metabolite‐mediated strategies to selectively recruit beneficial microorganisms in their microbiota. Some of these microbiota members show host‐adaptation, from which mutualism may rapidly arise. In the holobiont, microbiota members also co‐evolved antagonistic activities that restrict proliferation of microbes with high pathogenic potential and can therefore prevent disease development. Co‐evolution within holobionts thus ultimately drives plant performance. John Wiley and Sons Inc. 2023-07-20 /pmc/articles/PMC10481671/ /pubmed/37471099 http://dx.doi.org/10.15252/embr.202357455 Text en © 2023 The Authors. Published under the terms of the CC BY 4.0 license. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Reviews
Mesny, Fantin
Hacquard, Stéphane
Thomma, Bart PHJ
Co‐evolution within the plant holobiont drives host performance
title Co‐evolution within the plant holobiont drives host performance
title_full Co‐evolution within the plant holobiont drives host performance
title_fullStr Co‐evolution within the plant holobiont drives host performance
title_full_unstemmed Co‐evolution within the plant holobiont drives host performance
title_short Co‐evolution within the plant holobiont drives host performance
title_sort co‐evolution within the plant holobiont drives host performance
topic Reviews
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10481671/
https://www.ncbi.nlm.nih.gov/pubmed/37471099
http://dx.doi.org/10.15252/embr.202357455
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