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Microbe-associated molecular pattern recognition receptors have little effect on endophytic Arabidopsis thaliana microbiome assembly in the field

Plant microbiome structure affects plant health and productivity. A limited subset of environmental microbes successfully establishes within plant tissues, but the forces underlying this selectivity remain poorly characterized. Transmembrane pattern recognition receptors (PRRs), used by plants to de...

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Autores principales: Oldstone-Jackson, Caroline, Huang, Feng, Bergelson, Joy
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10663345/
https://www.ncbi.nlm.nih.gov/pubmed/38023837
http://dx.doi.org/10.3389/fpls.2023.1276472
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author Oldstone-Jackson, Caroline
Huang, Feng
Bergelson, Joy
author_facet Oldstone-Jackson, Caroline
Huang, Feng
Bergelson, Joy
author_sort Oldstone-Jackson, Caroline
collection PubMed
description Plant microbiome structure affects plant health and productivity. A limited subset of environmental microbes successfully establishes within plant tissues, but the forces underlying this selectivity remain poorly characterized. Transmembrane pattern recognition receptors (PRRs), used by plants to detect microbe-associated molecular patterns (MAMPs), are strong candidates for achieving this selectivity because PRRs can potentially interact with many members of the microbiome. Indeed, MAMPs found in many microbial taxa, including beneficials and commensals, can instigate a robust immune response that affects microbial growth. Surprisingly, we found that MAMP-detecting PRRs have little effect on endophytic bacterial and fungal microbiome structure in the field. We compared the microbiomes of four PRR knockout lines of Arabidopsis thaliana to wild-type plants in multiple tissue types over several developmental stages and detected only subtle shifts in fungal, but not bacterial, β-diversity in one of the four PRR mutants. In one developmental stage, lore mutants had slightly altered fungal β-diversity, indicating that LORE may be involved in plant-fungal interactions in addition to its known role in detecting certain bacterial lipids. No other effects of PRRs on α-diversity, microbiome variability, within-individual homogeneity, or microbial load were found. The general lack of effect suggests that individual MAMP-detecting PRRs are not critical in shaping the endophytic plant microbiome. Rather, we suggest that MAMP-detecting PRRs must either act in concert and/or are individually maintained through pleiotropic effects or interactions with coevolved mutualists or pathogens. Although unexpected, these results offer insights into the role of MAMP-detecting PRRs in plant-microbe interactions and help direct future efforts to uncover host genetic elements that control plant microbiome assembly.
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spelling pubmed-106633452023-01-01 Microbe-associated molecular pattern recognition receptors have little effect on endophytic Arabidopsis thaliana microbiome assembly in the field Oldstone-Jackson, Caroline Huang, Feng Bergelson, Joy Front Plant Sci Plant Science Plant microbiome structure affects plant health and productivity. A limited subset of environmental microbes successfully establishes within plant tissues, but the forces underlying this selectivity remain poorly characterized. Transmembrane pattern recognition receptors (PRRs), used by plants to detect microbe-associated molecular patterns (MAMPs), are strong candidates for achieving this selectivity because PRRs can potentially interact with many members of the microbiome. Indeed, MAMPs found in many microbial taxa, including beneficials and commensals, can instigate a robust immune response that affects microbial growth. Surprisingly, we found that MAMP-detecting PRRs have little effect on endophytic bacterial and fungal microbiome structure in the field. We compared the microbiomes of four PRR knockout lines of Arabidopsis thaliana to wild-type plants in multiple tissue types over several developmental stages and detected only subtle shifts in fungal, but not bacterial, β-diversity in one of the four PRR mutants. In one developmental stage, lore mutants had slightly altered fungal β-diversity, indicating that LORE may be involved in plant-fungal interactions in addition to its known role in detecting certain bacterial lipids. No other effects of PRRs on α-diversity, microbiome variability, within-individual homogeneity, or microbial load were found. The general lack of effect suggests that individual MAMP-detecting PRRs are not critical in shaping the endophytic plant microbiome. Rather, we suggest that MAMP-detecting PRRs must either act in concert and/or are individually maintained through pleiotropic effects or interactions with coevolved mutualists or pathogens. Although unexpected, these results offer insights into the role of MAMP-detecting PRRs in plant-microbe interactions and help direct future efforts to uncover host genetic elements that control plant microbiome assembly. Frontiers Media S.A. 2023-11-08 /pmc/articles/PMC10663345/ /pubmed/38023837 http://dx.doi.org/10.3389/fpls.2023.1276472 Text en Copyright © 2023 Oldstone-Jackson, Huang and Bergelson https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Oldstone-Jackson, Caroline
Huang, Feng
Bergelson, Joy
Microbe-associated molecular pattern recognition receptors have little effect on endophytic Arabidopsis thaliana microbiome assembly in the field
title Microbe-associated molecular pattern recognition receptors have little effect on endophytic Arabidopsis thaliana microbiome assembly in the field
title_full Microbe-associated molecular pattern recognition receptors have little effect on endophytic Arabidopsis thaliana microbiome assembly in the field
title_fullStr Microbe-associated molecular pattern recognition receptors have little effect on endophytic Arabidopsis thaliana microbiome assembly in the field
title_full_unstemmed Microbe-associated molecular pattern recognition receptors have little effect on endophytic Arabidopsis thaliana microbiome assembly in the field
title_short Microbe-associated molecular pattern recognition receptors have little effect on endophytic Arabidopsis thaliana microbiome assembly in the field
title_sort microbe-associated molecular pattern recognition receptors have little effect on endophytic arabidopsis thaliana microbiome assembly in the field
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10663345/
https://www.ncbi.nlm.nih.gov/pubmed/38023837
http://dx.doi.org/10.3389/fpls.2023.1276472
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