Pioneer Arabidopsis thaliana spans the succession gradient revealing a diverse root-associated microbiome

Abstract Background Soil microbiomes are increasingly acknowledged to affect plant functioning. Research in molecular model species Arabidopsis thaliana has given detailed insights of such plant-microbiome interactions. However, the circumstances under which natural A. thaliana plants have been stud...

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Main Authors: Vera Hesen, Yvet Boele, Tanja Bakx-Schotman, Femke van Beersum, Ciska Raaijmakers, Ben Scheres, Viola Willemsen, Wim H. van der Putten
Format: Article
Language:English
Published: BMC 2023-07-01
Series:Environmental Microbiome
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Online Access:https://doi.org/10.1186/s40793-023-00511-y
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author Vera Hesen
Yvet Boele
Tanja Bakx-Schotman
Femke van Beersum
Ciska Raaijmakers
Ben Scheres
Viola Willemsen
Wim H. van der Putten
author_facet Vera Hesen
Yvet Boele
Tanja Bakx-Schotman
Femke van Beersum
Ciska Raaijmakers
Ben Scheres
Viola Willemsen
Wim H. van der Putten
author_sort Vera Hesen
collection DOAJ
description Abstract Background Soil microbiomes are increasingly acknowledged to affect plant functioning. Research in molecular model species Arabidopsis thaliana has given detailed insights of such plant-microbiome interactions. However, the circumstances under which natural A. thaliana plants have been studied so far might represent only a subset of A. thaliana’s full ecological context and potential biotic diversity of its root-associated microbiome. Results We collected A. thaliana root-associated soils from a secondary succession gradient covering 40 years of land abandonment. All field sites were situated on the same parent soil material and in the same climatic region. By sequencing the bacterial and fungal communities and soil abiotic analysis we discovered differences in both the biotic and abiotic composition of the root-associated soil of A. thaliana and these differences are in accordance with the successional class of the field sites. As the studied sites all have been under (former) agricultural use, and a climatic cline is absent, we were able to reveal a more complete variety of ecological contexts A. thaliana can appear and sustain in. Conclusions Our findings lead to the conclusion that although A. thaliana is considered a pioneer plant species and previously almost exclusively studied in early succession and disturbed sites, plants can successfully establish in soils which have experienced years of ecological development. Thereby, A. thaliana can be exposed to a much wider variation in soil ecological context than is currently presumed. This knowledge opens up new opportunities to enhance our understanding of causal plant-microbiome interactions as A. thaliana cannot only grow in contrasting soil biotic and abiotic conditions along a latitudinal gradient, but also when those conditions vary along a secondary succession gradient. Future research could give insights in important plant factors to grow in more ecologically complex later-secondary succession soils, which is an impending direction of our current agricultural systems.
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spelling doaj.art-669ef962352b4792a8a1d48f16209bb12023-07-23T11:26:57ZengBMCEnvironmental Microbiome2524-63722023-07-0118111110.1186/s40793-023-00511-yPioneer Arabidopsis thaliana spans the succession gradient revealing a diverse root-associated microbiomeVera Hesen0Yvet Boele1Tanja Bakx-Schotman2Femke van Beersum3Ciska Raaijmakers4Ben Scheres5Viola Willemsen6Wim H. van der Putten7Cluster of Plant Developmental Biology, Laboratory of Molecular Biology, Wageningen UniversityCluster of Plant Developmental Biology, Laboratory of Molecular Biology, Wageningen UniversityDepartment of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW)Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW)Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW)Cluster of Plant Developmental Biology, Laboratory of Molecular Biology, Wageningen UniversityCluster of Plant Developmental Biology, Laboratory of Molecular Biology, Wageningen UniversityDepartment of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW)Abstract Background Soil microbiomes are increasingly acknowledged to affect plant functioning. Research in molecular model species Arabidopsis thaliana has given detailed insights of such plant-microbiome interactions. However, the circumstances under which natural A. thaliana plants have been studied so far might represent only a subset of A. thaliana’s full ecological context and potential biotic diversity of its root-associated microbiome. Results We collected A. thaliana root-associated soils from a secondary succession gradient covering 40 years of land abandonment. All field sites were situated on the same parent soil material and in the same climatic region. By sequencing the bacterial and fungal communities and soil abiotic analysis we discovered differences in both the biotic and abiotic composition of the root-associated soil of A. thaliana and these differences are in accordance with the successional class of the field sites. As the studied sites all have been under (former) agricultural use, and a climatic cline is absent, we were able to reveal a more complete variety of ecological contexts A. thaliana can appear and sustain in. Conclusions Our findings lead to the conclusion that although A. thaliana is considered a pioneer plant species and previously almost exclusively studied in early succession and disturbed sites, plants can successfully establish in soils which have experienced years of ecological development. Thereby, A. thaliana can be exposed to a much wider variation in soil ecological context than is currently presumed. This knowledge opens up new opportunities to enhance our understanding of causal plant-microbiome interactions as A. thaliana cannot only grow in contrasting soil biotic and abiotic conditions along a latitudinal gradient, but also when those conditions vary along a secondary succession gradient. Future research could give insights in important plant factors to grow in more ecologically complex later-secondary succession soils, which is an impending direction of our current agricultural systems.https://doi.org/10.1186/s40793-023-00511-ySecondary successionSoilBacteriaFungiChronosequence
spellingShingle Vera Hesen
Yvet Boele
Tanja Bakx-Schotman
Femke van Beersum
Ciska Raaijmakers
Ben Scheres
Viola Willemsen
Wim H. van der Putten
Pioneer Arabidopsis thaliana spans the succession gradient revealing a diverse root-associated microbiome
Environmental Microbiome
Secondary succession
Soil
Bacteria
Fungi
Chronosequence
title Pioneer Arabidopsis thaliana spans the succession gradient revealing a diverse root-associated microbiome
title_full Pioneer Arabidopsis thaliana spans the succession gradient revealing a diverse root-associated microbiome
title_fullStr Pioneer Arabidopsis thaliana spans the succession gradient revealing a diverse root-associated microbiome
title_full_unstemmed Pioneer Arabidopsis thaliana spans the succession gradient revealing a diverse root-associated microbiome
title_short Pioneer Arabidopsis thaliana spans the succession gradient revealing a diverse root-associated microbiome
title_sort pioneer arabidopsis thaliana spans the succession gradient revealing a diverse root associated microbiome
topic Secondary succession
Soil
Bacteria
Fungi
Chronosequence
url https://doi.org/10.1186/s40793-023-00511-y
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