Phytochrome-mediated shade avoidance responses impact the structure and composition of the bacterial phyllosphere microbiome of Arabidopsis

Abstract The shade avoidance response triggers a dramatic promotion of elongation growth, accompanied by a significant reprogramming of metabolic pathways as plants seek to prevent overtopping and adapt to vegetative shade. Here we demonstrate that simulated vegetative shade results in significant c...

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Main Authors: James A. O’Rourke, Stacey A. Vincent, Isabel E. I. Williams, Eleanor L. Gascoyne, Paul F. Devlin
Format: Article
Language:English
Published: BMC 2025-02-01
Series:Environmental Microbiome
Subjects:
Online Access:https://doi.org/10.1186/s40793-025-00679-5
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author James A. O’Rourke
Stacey A. Vincent
Isabel E. I. Williams
Eleanor L. Gascoyne
Paul F. Devlin
author_facet James A. O’Rourke
Stacey A. Vincent
Isabel E. I. Williams
Eleanor L. Gascoyne
Paul F. Devlin
author_sort James A. O’Rourke
collection DOAJ
description Abstract The shade avoidance response triggers a dramatic promotion of elongation growth, accompanied by a significant reprogramming of metabolic pathways as plants seek to prevent overtopping and adapt to vegetative shade. Here we demonstrate that simulated vegetative shade results in significant changes in the structure and composition of the phyllosphere bacterial microbiome. Our study uncovered significant shifts in the diversity, occurrence, abundance and activity of bacteria within the phyllosphere microbiome. A comparison of responses in both wild-type plants and phytochrome mutants, which inherently exhibit a shade-avoidance phenotype, revealed both indirect responses to host plant physiology and direct responses to light among the microbiota. Hierarchical clustering of response patterns further suggested that over a third of the taxa constituting the core phyllosphere microbiome in our assay show some degree of response to vegetative shade. Bacteria that increased in abundance on plants with a shade-avoidance phenotype corresponded to genera associated with beneficial traits such as enhanced disease resistance and growth promotion. Our findings suggests that plants manipulate their phyllosphere microbiome under shade conditions as a strategy to optimise fitness when competing for light. We discuss the implications of our findings in terms of furthering our understanding of plant-microbe signalling in the shaping of the phyllosphere microbiome and the possibility of manipulating the phyllosphere microbiome for plant health in an agricultural setting at high planting densities.
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institution Kabale University
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spelling doaj-art-634062e51d234f218a01a744c091346d2025-02-09T12:55:09ZengBMCEnvironmental Microbiome2524-63722025-02-0120111510.1186/s40793-025-00679-5Phytochrome-mediated shade avoidance responses impact the structure and composition of the bacterial phyllosphere microbiome of ArabidopsisJames A. O’Rourke0Stacey A. Vincent1Isabel E. I. Williams2Eleanor L. Gascoyne3Paul F. Devlin4Department of Biological Sciences, Royal Holloway University of LondonDepartment of Biological Sciences, Royal Holloway University of LondonDepartment of Biological Sciences, Royal Holloway University of LondonDepartment of Biological Sciences, Royal Holloway University of LondonDepartment of Biological Sciences, Royal Holloway University of LondonAbstract The shade avoidance response triggers a dramatic promotion of elongation growth, accompanied by a significant reprogramming of metabolic pathways as plants seek to prevent overtopping and adapt to vegetative shade. Here we demonstrate that simulated vegetative shade results in significant changes in the structure and composition of the phyllosphere bacterial microbiome. Our study uncovered significant shifts in the diversity, occurrence, abundance and activity of bacteria within the phyllosphere microbiome. A comparison of responses in both wild-type plants and phytochrome mutants, which inherently exhibit a shade-avoidance phenotype, revealed both indirect responses to host plant physiology and direct responses to light among the microbiota. Hierarchical clustering of response patterns further suggested that over a third of the taxa constituting the core phyllosphere microbiome in our assay show some degree of response to vegetative shade. Bacteria that increased in abundance on plants with a shade-avoidance phenotype corresponded to genera associated with beneficial traits such as enhanced disease resistance and growth promotion. Our findings suggests that plants manipulate their phyllosphere microbiome under shade conditions as a strategy to optimise fitness when competing for light. We discuss the implications of our findings in terms of furthering our understanding of plant-microbe signalling in the shaping of the phyllosphere microbiome and the possibility of manipulating the phyllosphere microbiome for plant health in an agricultural setting at high planting densities.https://doi.org/10.1186/s40793-025-00679-5PhytochromeShade avoidancePhyllosphereMicrobiomeArabidopsis
spellingShingle James A. O’Rourke
Stacey A. Vincent
Isabel E. I. Williams
Eleanor L. Gascoyne
Paul F. Devlin
Phytochrome-mediated shade avoidance responses impact the structure and composition of the bacterial phyllosphere microbiome of Arabidopsis
Environmental Microbiome
Phytochrome
Shade avoidance
Phyllosphere
Microbiome
Arabidopsis
title Phytochrome-mediated shade avoidance responses impact the structure and composition of the bacterial phyllosphere microbiome of Arabidopsis
title_full Phytochrome-mediated shade avoidance responses impact the structure and composition of the bacterial phyllosphere microbiome of Arabidopsis
title_fullStr Phytochrome-mediated shade avoidance responses impact the structure and composition of the bacterial phyllosphere microbiome of Arabidopsis
title_full_unstemmed Phytochrome-mediated shade avoidance responses impact the structure and composition of the bacterial phyllosphere microbiome of Arabidopsis
title_short Phytochrome-mediated shade avoidance responses impact the structure and composition of the bacterial phyllosphere microbiome of Arabidopsis
title_sort phytochrome mediated shade avoidance responses impact the structure and composition of the bacterial phyllosphere microbiome of arabidopsis
topic Phytochrome
Shade avoidance
Phyllosphere
Microbiome
Arabidopsis
url https://doi.org/10.1186/s40793-025-00679-5
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