Interactions between below‐ground traits and rhizosheath fungal and bacterial communities for phosphorus acquisition

Plant–soil–microbe interactions play a central role in plant nutrient acquisition and thus ecosystem functioning and nutrient availability in agroecosystems. Adjustments in root morphology, root exudation and associations with micro‐organisms such as arbuscular mycorrhizal fungi are common for phosp...

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Published inFunctional ecology Vol. 35; no. 7; pp. 1603 - 1619
Main Authors Honvault, Nicolas, Houben, David, Firmin, Stéphane, Meglouli, Hacène, Laruelle, Frédéric, Fontaine, Joël, Lounès‐Hadj Sahraoui, Anissa, Coutu, Arnaud, Lambers, Hans, Faucon, Michel‐Pierre
Format Journal Article
LanguageEnglish
Published London Wiley Subscription Services, Inc 01.07.2021
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Abstract Plant–soil–microbe interactions play a central role in plant nutrient acquisition and thus ecosystem functioning and nutrient availability in agroecosystems. Adjustments in root morphology, root exudation and associations with micro‐organisms such as arbuscular mycorrhizal fungi are common for phosphorus acquisition. Yet how plant below‐ground functional traits interact with microbial communities for P acquisition remains largely unknown, limiting our understanding of phosphorus availability in agroecosystems. Interactions between below‐ground functional traits and rhizosheath soil microbial communities for P acquisition were investigated across eight herbaceous species with contrasting root traits. Root morphological and physiological traits involved in P acquisition were quantified simultaneously with PLFA (phospholipid fatty acid) and NLFA (neutral lipid fatty acid) microbial bioindicators. Multiple correlations were observed between root morphology, root exudates and rhizosheath fungal and bacterial communities. Root exudates and in particular release of malate and malonate were strongly linked with indicators of Gram‐negative bacteria, which were correlated with changes in rhizosheath soil P concentration and plant P content. Our results suggest that root exudation of carboxylates may play an important role in plant–soil–microbe interactions for P acquisition, underlining their likely role in shaping microbial communities. Incorporating these interactions in biogeochemical models would lead to better predicting power and understanding of P cycling and ecosystem functioning. A free Plain Language Summary can be found within the Supporting Information of this article. Résumé Les interactions plante‐sol‐microbe jouent un rôle central dans l'acquisition d’éléments nutritifs par les plantes et par conséquent dans le fonctionnement des écosystèmes et la disponibilité des nutriments dans les agroécosystèmes. L’acquisition du phosphore nécessite souvent des ajustements entre morphologie et exsudations racinaires ainsi que l'association des racines avec les micro‐organismes du sol tels que les champignons mycorhiziens arbusculaires. Les mécanismes par lesquels les traits fonctionnels des plantes interagissent avec les communautés microbiennes pour l'acquisition de P restent pourtant largement méconnus, limitant ainsi notre compréhension de la disponibilité du phosphore dans les agroécosystèmes. Les interactions entre traits fonctionnels souterrains et communautés microbiennes du sol rhizosphérique pour l'acquisition de P ont été étudiées au sein de huit espèces herbacées aux traits racinaires contrastés. De multiples traits morphologiques et physiologiques racinaires impliqués dans l'acquisition de P ont été quantifiés simultanément avec plusieurs bioindicateurs microbiens (PLFA et NLFA). De nombreuses corrélations ont été observées entre la morphologie racinaire, les exsudats racinaires et les communautés fongiques et bactériennes du sol rhizosphérique. Les exsudats racinaires, en particulier la libération d'acide malique et malonique, étaient fortement liés aux indicateurs de bactéries Gram‐négatives, eux‐mêmes corrélés aux changements de la concentration en P du sol rhizosphérique et à la teneur en P des plantes. Nos résultats suggèrent que l'exsudation racinaire des carboxylates joue un rôle important dans les interactions plante‐sol‐microbe pour l'acquisition de P, soulignant leur rôle probable dans la formation des communautés microbiennes. L'intégration de ces interactions dans les modèles biogéochimiques conduirait à une meilleure précision ainsi qu’à une meilleure compréhension du cycle du P et du fonctionnement des écosystèmes. A free Plain Language Summary can be found within the Supporting Information of this article.
AbstractList Plant–soil–microbe interactions play a central role in plant nutrient acquisition and thus ecosystem functioning and nutrient availability in agroecosystems. Adjustments in root morphology, root exudation and associations with micro‐organisms such as arbuscular mycorrhizal fungi are common for phosphorus acquisition. Yet how plant below‐ground functional traits interact with microbial communities for P acquisition remains largely unknown, limiting our understanding of phosphorus availability in agroecosystems.Interactions between below‐ground functional traits and rhizosheath soil microbial communities for P acquisition were investigated across eight herbaceous species with contrasting root traits. Root morphological and physiological traits involved in P acquisition were quantified simultaneously with PLFA (phospholipid fatty acid) and NLFA (neutral lipid fatty acid) microbial bioindicators.Multiple correlations were observed between root morphology, root exudates and rhizosheath fungal and bacterial communities. Root exudates and in particular release of malate and malonate were strongly linked with indicators of Gram‐negative bacteria, which were correlated with changes in rhizosheath soil P concentration and plant P content.Our results suggest that root exudation of carboxylates may play an important role in plant–soil–microbe interactions for P acquisition, underlining their likely role in shaping microbial communities. Incorporating these interactions in biogeochemical models would lead to better predicting power and understanding of P cycling and ecosystem functioning.A free Plain Language Summary can be found within the Supporting Information of this article.
Plant–soil–microbe interactions play a central role in plant nutrient acquisition and thus ecosystem functioning and nutrient availability in agroecosystems. Adjustments in root morphology, root exudation and associations with micro‐organisms such as arbuscular mycorrhizal fungi are common for phosphorus acquisition. Yet how plant below‐ground functional traits interact with microbial communities for P acquisition remains largely unknown, limiting our understanding of phosphorus availability in agroecosystems. Interactions between below‐ground functional traits and rhizosheath soil microbial communities for P acquisition were investigated across eight herbaceous species with contrasting root traits. Root morphological and physiological traits involved in P acquisition were quantified simultaneously with PLFA (phospholipid fatty acid) and NLFA (neutral lipid fatty acid) microbial bioindicators. Multiple correlations were observed between root morphology, root exudates and rhizosheath fungal and bacterial communities. Root exudates and in particular release of malate and malonate were strongly linked with indicators of Gram‐negative bacteria, which were correlated with changes in rhizosheath soil P concentration and plant P content. Our results suggest that root exudation of carboxylates may play an important role in plant–soil–microbe interactions for P acquisition, underlining their likely role in shaping microbial communities. Incorporating these interactions in biogeochemical models would lead to better predicting power and understanding of P cycling and ecosystem functioning. A free Plain Language Summary can be found within the Supporting Information of this article. Résumé Les interactions plante‐sol‐microbe jouent un rôle central dans l'acquisition d’éléments nutritifs par les plantes et par conséquent dans le fonctionnement des écosystèmes et la disponibilité des nutriments dans les agroécosystèmes. L’acquisition du phosphore nécessite souvent des ajustements entre morphologie et exsudations racinaires ainsi que l'association des racines avec les micro‐organismes du sol tels que les champignons mycorhiziens arbusculaires. Les mécanismes par lesquels les traits fonctionnels des plantes interagissent avec les communautés microbiennes pour l'acquisition de P restent pourtant largement méconnus, limitant ainsi notre compréhension de la disponibilité du phosphore dans les agroécosystèmes. Les interactions entre traits fonctionnels souterrains et communautés microbiennes du sol rhizosphérique pour l'acquisition de P ont été étudiées au sein de huit espèces herbacées aux traits racinaires contrastés. De multiples traits morphologiques et physiologiques racinaires impliqués dans l'acquisition de P ont été quantifiés simultanément avec plusieurs bioindicateurs microbiens (PLFA et NLFA). De nombreuses corrélations ont été observées entre la morphologie racinaire, les exsudats racinaires et les communautés fongiques et bactériennes du sol rhizosphérique. Les exsudats racinaires, en particulier la libération d'acide malique et malonique, étaient fortement liés aux indicateurs de bactéries Gram‐négatives, eux‐mêmes corrélés aux changements de la concentration en P du sol rhizosphérique et à la teneur en P des plantes. Nos résultats suggèrent que l'exsudation racinaire des carboxylates joue un rôle important dans les interactions plante‐sol‐microbe pour l'acquisition de P, soulignant leur rôle probable dans la formation des communautés microbiennes. L'intégration de ces interactions dans les modèles biogéochimiques conduirait à une meilleure précision ainsi qu’à une meilleure compréhension du cycle du P et du fonctionnement des écosystèmes. A free Plain Language Summary can be found within the Supporting Information of this article.
Plant–soil–microbe interactions play a central role in plant nutrient acquisition and thus ecosystem functioning and nutrient availability in agroecosystems. Adjustments in root morphology, root exudation and associations with micro‐organisms such as arbuscular mycorrhizal fungi are common for phosphorus acquisition. Yet how plant below‐ground functional traits interact with microbial communities for P acquisition remains largely unknown, limiting our understanding of phosphorus availability in agroecosystems. Interactions between below‐ground functional traits and rhizosheath soil microbial communities for P acquisition were investigated across eight herbaceous species with contrasting root traits. Root morphological and physiological traits involved in P acquisition were quantified simultaneously with PLFA (phospholipid fatty acid) and NLFA (neutral lipid fatty acid) microbial bioindicators. Multiple correlations were observed between root morphology, root exudates and rhizosheath fungal and bacterial communities. Root exudates and in particular release of malate and malonate were strongly linked with indicators of Gram‐negative bacteria, which were correlated with changes in rhizosheath soil P concentration and plant P content. Our results suggest that root exudation of carboxylates may play an important role in plant–soil–microbe interactions for P acquisition, underlining their likely role in shaping microbial communities. Incorporating these interactions in biogeochemical models would lead to better predicting power and understanding of P cycling and ecosystem functioning. A free Plain Language Summary can be found within the Supporting Information of this article. Les interactions plante‐sol‐microbe jouent un rôle central dans l'acquisition d’éléments nutritifs par les plantes et par conséquent dans le fonctionnement des écosystèmes et la disponibilité des nutriments dans les agroécosystèmes. L’acquisition du phosphore nécessite souvent des ajustements entre morphologie et exsudations racinaires ainsi que l'association des racines avec les micro‐organismes du sol tels que les champignons mycorhiziens arbusculaires. Les mécanismes par lesquels les traits fonctionnels des plantes interagissent avec les communautés microbiennes pour l'acquisition de P restent pourtant largement méconnus, limitant ainsi notre compréhension de la disponibilité du phosphore dans les agroécosystèmes. Les interactions entre traits fonctionnels souterrains et communautés microbiennes du sol rhizosphérique pour l'acquisition de P ont été étudiées au sein de huit espèces herbacées aux traits racinaires contrastés. De multiples traits morphologiques et physiologiques racinaires impliqués dans l'acquisition de P ont été quantifiés simultanément avec plusieurs bioindicateurs microbiens (PLFA et NLFA). De nombreuses corrélations ont été observées entre la morphologie racinaire, les exsudats racinaires et les communautés fongiques et bactériennes du sol rhizosphérique. Les exsudats racinaires, en particulier la libération d'acide malique et malonique, étaient fortement liés aux indicateurs de bactéries Gram‐négatives, eux‐mêmes corrélés aux changements de la concentration en P du sol rhizosphérique et à la teneur en P des plantes. Nos résultats suggèrent que l'exsudation racinaire des carboxylates joue un rôle important dans les interactions plante‐sol‐microbe pour l'acquisition de P, soulignant leur rôle probable dans la formation des communautés microbiennes. L'intégration de ces interactions dans les modèles biogéochimiques conduirait à une meilleure précision ainsi qu’à une meilleure compréhension du cycle du P et du fonctionnement des écosystèmes.
1. Plant-soil-microbe interactions play a central role in plant nutrient acquisitionand thus ecosystem functioning and nutrient availability in agroecosystems.Adjustments in root morphology, root exudation and associations withmicroorganisms such as arbuscular mychorrizal fungi are common forphosphorus acquisition. Yet how plant belowground functional traits interactwith microbial communities for P-acquisition remains largely unknown, limitingour understanding of phosphorus availability in agroecosystems.2. Interactions between belowground functional traits and rhizosheath soilmicrobial communities for P-acquisition were investigated across eightherbaceous species with contrasting root traits. Root morphological andphysiological traits involved in P-acquisition were quantified simultaneouslywith PLFA (phospholipid fatty acid) and NLFA (neutral lipid fatty acid)microbial bioindicators.3. Multiple correlations were observed between root morphology, root exudatesand rhizosheath fungal and bacterial communities. Root exudates and inparticular release of malate and malonate were strongly linked with indicatorsof Gram-negative bacteria, which were correlated with changes in rhizosheathsoil P concentration and plant P content.4. Our results suggest that root exudation of carboxylates may play an importantrole in plant-soil-microbe interactions for P-acquisition, underlining their likelyrole in shaping microbial communities. Incorporating these interactions inbiogeochemical models would lead to better predicting power andunderstanding of P cycling and ecosystem functioning. 1. Les interactions plante-sol-microbe jouent un rôle central dans l'acquisitiond’éléments nutritifs par les plantes et par conséquent dans le fonctionnementdes écosystèmes et la disponibilité des nutriments dans lesagroécosystèmes. L’acquisition du phosphore nécessite souvent desajustements entre morphologie et exsudations racinaires ainsi quel’association des racines avec les micro-organismes du sol tels que leschampignons mycorhiziens arbusculaires. Les mécanismes par lesquels lestraits fonctionnels des plantes interagissent avec les communautésmicrobiennes pour l'acquisition de P restent pourtant largement méconnus,limitant ainsi notre compréhension de la disponibilité du phosphore dans lesagroécosystèmes.2. Les interactions entre traits fonctionnels souterrains et communautésmicrobiennes du sol rhizosphérique pour l'acquisition de P ont été étudiées ausein de huit espèces herbacées aux traits racinaires contrastés. De multiplestraits morphologiques et physiologiques racinaires impliqués dans l'acquisitionde P ont été quantifiés simultanément avec plusieurs bioindicateursmicrobiens (PLFA et NLFA).3. De nombreuses corrélations ont été observées entre la morphologie racinaire,les exsudats racinaires et les communautés fongiques et bactériennes du solrhizosphérique. Les exsudats racinaires, en particulier la libération d’acidemalique et malonique, étaient fortement liés aux indicateurs de bactériesGram-négatives, eux-mêmes corrélés aux changements de la concentrationen P du sol rhizosphérique et à la teneur en P des plantes.4. Nos résultats suggèrent que l'exsudation racinaire des carboxylates joue unrôle important dans les interactions plante-sol-microbe pour l'acquisition de P,soulignant leur rôle probable dans la formation des communautésmicrobiennes. L'intégration de ces interactions dans les modèlesbiogéochimiques conduirait à une meilleure précision ainsi qu’à une meilleurecompréhension du cycle du P et du fonctionnement des écosystèmes.
Author Lambers, Hans
Faucon, Michel‐Pierre
Coutu, Arnaud
Meglouli, Hacène
Firmin, Stéphane
Fontaine, Joël
Honvault, Nicolas
Houben, David
Laruelle, Frédéric
Lounès‐Hadj Sahraoui, Anissa
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  givenname: David
  surname: Houben
  fullname: Houben, David
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  surname: Firmin
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  organization: UniLaSalle
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  surname: Meglouli
  fullname: Meglouli, Hacène
  organization: Université de Montréal
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  surname: Lounès‐Hadj Sahraoui
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  givenname: Hans
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  surname: Lambers
  fullname: Lambers, Hans
  organization: University of Western Australia
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  givenname: Michel‐Pierre
  orcidid: 0000-0001-5448-7932
  surname: Faucon
  fullname: Faucon, Michel‐Pierre
  email: michel-pierre.faucon@unilasalle.fr
  organization: UniLaSalle
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Issue 7
Keywords PLFA
phosphorus acquisition
NLFA
plant-soil microbe interactions
Language English
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Snippet Plant–soil–microbe interactions play a central role in plant nutrient acquisition and thus ecosystem functioning and nutrient availability in agroecosystems....
1. Plant-soil-microbe interactions play a central role in plant nutrient acquisitionand thus ecosystem functioning and nutrient availability in...
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SubjectTerms Agricultural ecosystems
agroecosystems
Arbuscular mycorrhizas
Availability
Bacteria
Bioindicators
Carboxylates
Exudates
Exudation
Fatty acids
Fungi
Gram-negative bacteria
herbaceous plants
Indicator species
Life Sciences
Lipids
Malate
malates
Microbial activity
Microorganisms
Morphology
neutral lipid fatty acid
Nutrient availability
phospholipid fatty acid
phospholipid fatty acids
Phospholipids
Phosphorus
phosphorus acquisition
plant–soil–microbe interactions
soil
Soil investigations
Soils
vesicular arbuscular mycorrhizae
Title Interactions between below‐ground traits and rhizosheath fungal and bacterial communities for phosphorus acquisition
URI https://onlinelibrary.wiley.com/doi/abs/10.1111%2F1365-2435.13823
https://www.proquest.com/docview/2548786709
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https://hal.science/hal-03286269
Volume 35
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