Plant intraspecific variation modulates nutrient cycling through its below ground rhizospheric microbiome

Plant genetic variation, through its phenotypic display, can determine the composition of below ground microbial communities. Variation within a species is increasingly acknowledged to have substantial ecological consequences, particularly through trophic cascades. We hypothesized that the intraspecific genotypic variation of the tree host might impact the phylogenetic composition of its rhizospheric microbial communities, by favouring particular clades, that might be further reflected in ecosystem process rates. We tested whether the intraspecific genotypic variation of Pinus pinaster modulates nutrient cycling by determining the phylogenetic structure of its symbiotic ectomycorrhizal fungi and rhizospheric bacteria. We sequenced fungal and bacterial molecular markers and reconstructed phylogenies in the rhizosphere of P. pinaster trees belonging to three genotypic variants (Mediterranean, Atlantic, African) in three 45-year-old common garden experiments, and measured seven soil enzymatic activities. Local effects, based on differences in elevation and soil conditions across sites, were strong predictors of the ectomycorrhizal and bacterial communities thriving in tree’s rhizosphere. Across-site variation also explained differences in phosphorus cycling. We detected, however, a significant effect of the plant genotype on the phylogenetic structure of the root-associated microbiota that was consistent across sites. The most productive Mediterranean plant genotype sheltered the most distinct root microbiome, with the dominant Basidiomycetes and Proteobacteria having a strong influence on the phylogenetic microbial community structure and associating with an enhanced hydrolysis of celluloses, hemicelluloses and chitin. Beneath the less productive Atlantic genotype, the less abundant Ascomycetes and up to thirteen bacterial phyla shaped the phylogenetic microbial structure, and predicted the rates of peptidase. Ectomycorrhizal fungi explained the activity of cellulases and protease, and bacteria that of hemicellulases and chitinase, suggesting functional complementarity. Synthesis. This is the first report using three-replicated long-term common gardens in mature forests to disentangle plant genotype- and site-specific drivers of the rhizospheric microbiome and its enzymatic potential. We concluded that intraspecific variation in primary producers leaves a phylogenetic signature in mutualists and decomposers that further modulate key steps in carbon and nitrogen cycles. These results emphasize the ecological relevance of plant intraspecific diversity in determining essential plant–soil feedbacks that control ecosystem productivity and performance.

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Main Authors: Pérez-Izquierdo, Leticia, Zabal-Aguirre, M., González-Martínez, Santiago C., Buée, M, Verdú, Miguel, Rincón, A., Rincón, Ana, Goberna, M.
Other Authors: Ministerio de Economía y Competitividad (España)
Format: artículo biblioteca
Published: John Wiley & Sons 2019
Subjects:Ecosystem functioning, Ectomycorrhizal fungi, Nutrient cycling, Phylogenetic community structure, Plant genotype, Rhizosphere, Soil bacteria,
Online Access:http://hdl.handle.net/10261/201530
http://dx.doi.org/10.13039/501100003329
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id dig-cide-es-10261-201530
record_format koha
institution CIDE ES
collection DSpace
country España
countrycode ES
component Bibliográfico
access En linea
databasecode dig-cide-es
tag biblioteca
region Europa del Sur
libraryname Biblioteca del CIDE España
topic Ecosystem functioning
Ectomycorrhizal fungi
Nutrient cycling
Phylogenetic community structure
Plant genotype
Rhizosphere
Soil bacteria
Ecosystem functioning
Ectomycorrhizal fungi
Nutrient cycling
Phylogenetic community structure
Plant genotype
Rhizosphere
Soil bacteria
spellingShingle Ecosystem functioning
Ectomycorrhizal fungi
Nutrient cycling
Phylogenetic community structure
Plant genotype
Rhizosphere
Soil bacteria
Ecosystem functioning
Ectomycorrhizal fungi
Nutrient cycling
Phylogenetic community structure
Plant genotype
Rhizosphere
Soil bacteria
Pérez-Izquierdo, Leticia
Zabal-Aguirre, M.
González-Martínez, Santiago C.
Buée, M
Verdú, Miguel
Rincón, A.
Rincón, Ana
Goberna, M.
Plant intraspecific variation modulates nutrient cycling through its below ground rhizospheric microbiome
description Plant genetic variation, through its phenotypic display, can determine the composition of below ground microbial communities. Variation within a species is increasingly acknowledged to have substantial ecological consequences, particularly through trophic cascades. We hypothesized that the intraspecific genotypic variation of the tree host might impact the phylogenetic composition of its rhizospheric microbial communities, by favouring particular clades, that might be further reflected in ecosystem process rates. We tested whether the intraspecific genotypic variation of Pinus pinaster modulates nutrient cycling by determining the phylogenetic structure of its symbiotic ectomycorrhizal fungi and rhizospheric bacteria. We sequenced fungal and bacterial molecular markers and reconstructed phylogenies in the rhizosphere of P. pinaster trees belonging to three genotypic variants (Mediterranean, Atlantic, African) in three 45-year-old common garden experiments, and measured seven soil enzymatic activities. Local effects, based on differences in elevation and soil conditions across sites, were strong predictors of the ectomycorrhizal and bacterial communities thriving in tree’s rhizosphere. Across-site variation also explained differences in phosphorus cycling. We detected, however, a significant effect of the plant genotype on the phylogenetic structure of the root-associated microbiota that was consistent across sites. The most productive Mediterranean plant genotype sheltered the most distinct root microbiome, with the dominant Basidiomycetes and Proteobacteria having a strong influence on the phylogenetic microbial community structure and associating with an enhanced hydrolysis of celluloses, hemicelluloses and chitin. Beneath the less productive Atlantic genotype, the less abundant Ascomycetes and up to thirteen bacterial phyla shaped the phylogenetic microbial structure, and predicted the rates of peptidase. Ectomycorrhizal fungi explained the activity of cellulases and protease, and bacteria that of hemicellulases and chitinase, suggesting functional complementarity. Synthesis. This is the first report using three-replicated long-term common gardens in mature forests to disentangle plant genotype- and site-specific drivers of the rhizospheric microbiome and its enzymatic potential. We concluded that intraspecific variation in primary producers leaves a phylogenetic signature in mutualists and decomposers that further modulate key steps in carbon and nitrogen cycles. These results emphasize the ecological relevance of plant intraspecific diversity in determining essential plant–soil feedbacks that control ecosystem productivity and performance.
author2 Ministerio de Economía y Competitividad (España)
author_facet Ministerio de Economía y Competitividad (España)
Pérez-Izquierdo, Leticia
Zabal-Aguirre, M.
González-Martínez, Santiago C.
Buée, M
Verdú, Miguel
Rincón, A.
Rincón, Ana
Goberna, M.
format artículo
topic_facet Ecosystem functioning
Ectomycorrhizal fungi
Nutrient cycling
Phylogenetic community structure
Plant genotype
Rhizosphere
Soil bacteria
author Pérez-Izquierdo, Leticia
Zabal-Aguirre, M.
González-Martínez, Santiago C.
Buée, M
Verdú, Miguel
Rincón, A.
Rincón, Ana
Goberna, M.
author_sort Pérez-Izquierdo, Leticia
title Plant intraspecific variation modulates nutrient cycling through its below ground rhizospheric microbiome
title_short Plant intraspecific variation modulates nutrient cycling through its below ground rhizospheric microbiome
title_full Plant intraspecific variation modulates nutrient cycling through its below ground rhizospheric microbiome
title_fullStr Plant intraspecific variation modulates nutrient cycling through its below ground rhizospheric microbiome
title_full_unstemmed Plant intraspecific variation modulates nutrient cycling through its below ground rhizospheric microbiome
title_sort plant intraspecific variation modulates nutrient cycling through its below ground rhizospheric microbiome
publisher John Wiley & Sons
publishDate 2019
url http://hdl.handle.net/10261/201530
http://dx.doi.org/10.13039/501100003329
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spelling dig-cide-es-10261-2015302020-12-10T16:13:48Z Plant intraspecific variation modulates nutrient cycling through its below ground rhizospheric microbiome Pérez-Izquierdo, Leticia Zabal-Aguirre, M. González-Martínez, Santiago C. Buée, M Verdú, Miguel Rincón, A. Rincón, Ana Goberna, M. Ministerio de Economía y Competitividad (España) Pérez-Izquierdo, Leticia [0000-0002-5200-8157] Verdú, Miguel [0000-0002-9778-7692] Ecosystem functioning Ectomycorrhizal fungi Nutrient cycling Phylogenetic community structure Plant genotype Rhizosphere Soil bacteria Plant genetic variation, through its phenotypic display, can determine the composition of below ground microbial communities. Variation within a species is increasingly acknowledged to have substantial ecological consequences, particularly through trophic cascades. We hypothesized that the intraspecific genotypic variation of the tree host might impact the phylogenetic composition of its rhizospheric microbial communities, by favouring particular clades, that might be further reflected in ecosystem process rates. We tested whether the intraspecific genotypic variation of Pinus pinaster modulates nutrient cycling by determining the phylogenetic structure of its symbiotic ectomycorrhizal fungi and rhizospheric bacteria. We sequenced fungal and bacterial molecular markers and reconstructed phylogenies in the rhizosphere of P. pinaster trees belonging to three genotypic variants (Mediterranean, Atlantic, African) in three 45-year-old common garden experiments, and measured seven soil enzymatic activities. Local effects, based on differences in elevation and soil conditions across sites, were strong predictors of the ectomycorrhizal and bacterial communities thriving in tree’s rhizosphere. Across-site variation also explained differences in phosphorus cycling. We detected, however, a significant effect of the plant genotype on the phylogenetic structure of the root-associated microbiota that was consistent across sites. The most productive Mediterranean plant genotype sheltered the most distinct root microbiome, with the dominant Basidiomycetes and Proteobacteria having a strong influence on the phylogenetic microbial community structure and associating with an enhanced hydrolysis of celluloses, hemicelluloses and chitin. Beneath the less productive Atlantic genotype, the less abundant Ascomycetes and up to thirteen bacterial phyla shaped the phylogenetic microbial structure, and predicted the rates of peptidase. Ectomycorrhizal fungi explained the activity of cellulases and protease, and bacteria that of hemicellulases and chitinase, suggesting functional complementarity. Synthesis. This is the first report using three-replicated long-term common gardens in mature forests to disentangle plant genotype- and site-specific drivers of the rhizospheric microbiome and its enzymatic potential. We concluded that intraspecific variation in primary producers leaves a phylogenetic signature in mutualists and decomposers that further modulate key steps in carbon and nitrogen cycles. These results emphasize the ecological relevance of plant intraspecific diversity in determining essential plant–soil feedbacks that control ecosystem productivity and performance. This work was supported by the projects MyFUNCO (CGL2011‐29585‐C02‐02), and Microfac (CGL2014‐58333‐P) funded by the Spanish Ministry for Economy and Competitiveness (MINECO), as well as by the LABoratoire d'EXcellence Arbre (LABEX Arbre, INRA‐Nancy). L.P.‐I. held a pre‐doctoral fellowship and M.G. a Ramón y Cajal contract, both awarded by the Spanish Ministry of Economy and Competitiveness‐MINECO. 2020-02-21T11:34:41Z 2020-02-21T11:34:41Z 2019 2020-02-21T11:34:41Z artículo http://purl.org/coar/resource_type/c_6501 doi: 10.1111/1365-2745.13202 e-issn: 1365-2745 issn: 0022-0477 Journal of Ecology 107: 1594-1605 (2019) http://hdl.handle.net/10261/201530 10.1111/1365-2745.13202 http://dx.doi.org/10.13039/501100003329 #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/CGL2014-58333-P http://dx.doi.org/10.1111/1365-2745.13202 Sí none John Wiley & Sons