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Impact of Long-Term Organic and Mineral Fertilization on Rhizosphere Metabolites, Root–Microbial Interactions and Plant Health of Lettuce

Fertilization management can affect plant performance and soil microbiota, involving still poorly understood rhizosphere interactions. We hypothesized that fertilization practice exerts specific effects on rhizodeposition with consequences for recruitment of rhizosphere microbiota and plant performa...

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Autores principales: Windisch, Saskia, Sommermann, Loreen, Babin, Doreen, Chowdhury, Soumitra Paul, Grosch, Rita, Moradtalab, Narges, Walker, Frank, Höglinger, Birgit, El-Hasan, Abbas, Armbruster, Wolfgang, Nesme, Joseph, Sørensen, Søren Johannes, Schellenberg, Ingo, Geistlinger, Jörg, Smalla, Kornelia, Rothballer, Michael, Ludewig, Uwe, Neumann, Günter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7838544/
https://www.ncbi.nlm.nih.gov/pubmed/33519736
http://dx.doi.org/10.3389/fmicb.2020.597745
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author Windisch, Saskia
Sommermann, Loreen
Babin, Doreen
Chowdhury, Soumitra Paul
Grosch, Rita
Moradtalab, Narges
Walker, Frank
Höglinger, Birgit
El-Hasan, Abbas
Armbruster, Wolfgang
Nesme, Joseph
Sørensen, Søren Johannes
Schellenberg, Ingo
Geistlinger, Jörg
Smalla, Kornelia
Rothballer, Michael
Ludewig, Uwe
Neumann, Günter
author_facet Windisch, Saskia
Sommermann, Loreen
Babin, Doreen
Chowdhury, Soumitra Paul
Grosch, Rita
Moradtalab, Narges
Walker, Frank
Höglinger, Birgit
El-Hasan, Abbas
Armbruster, Wolfgang
Nesme, Joseph
Sørensen, Søren Johannes
Schellenberg, Ingo
Geistlinger, Jörg
Smalla, Kornelia
Rothballer, Michael
Ludewig, Uwe
Neumann, Günter
author_sort Windisch, Saskia
collection PubMed
description Fertilization management can affect plant performance and soil microbiota, involving still poorly understood rhizosphere interactions. We hypothesized that fertilization practice exerts specific effects on rhizodeposition with consequences for recruitment of rhizosphere microbiota and plant performance. To address this hypothesis, we conducted a minirhizotron experiment using lettuce as model plant and field soils with contrasting properties from two long-term field experiments (HUB-LTE: loamy sand, DOK-LTE: silty loam) with organic and mineral fertilization history. Increased relative abundance of plant-beneficial arbuscular mycorrhizal fungi and fungal pathotrophs were characteristic of the rhizospheres in the organically managed soils (HU-org; BIODYN2). Accordingly, defense-related genes were systemically expressed in shoot tissues of the respective plants. As a site-specific effect, high relative occurrence of the fungal lettuce pathogen Olpidium sp. (76–90%) was recorded in the rhizosphere, both under long-term organic and mineral fertilization at the DOK-LTE site, likely supporting Olpidium infection due to a lower water drainage potential compared to the sandy HUB-LTE soils. However, plant growth depressions and Olpidium infection were exclusively recorded in the BIODYN2 soil with organic fertilization history. This was associated with a drastic (87–97%) reduction in rhizosphere abundance of potentially plant-beneficial microbiota (Pseudomonadaceae, Mortierella elongata) and reduced concentrations of the antifungal root exudate benzoate, known to be increased in presence of Pseudomonas spp. In contrast, high relative abundance of Pseudomonadaceae (Gammaproteobacteria) in the rhizosphere of plants grown in soils with long-term mineral fertilization (61–74%) coincided with high rhizosphere concentrations of chemotactic dicarboxylates (succinate, malate) and a high C (sugar)/N (amino acid) ratio, known to support the growth of Gammaproteobacteria. This was related with generally lower systemic expression of plant defense genes as compared with organic fertilization history. Our results suggest a complex network of belowground interactions among root exudates, site-specific factors and rhizosphere microbiota, modulating the impact of fertilization management with consequences for plant health and performance.
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spelling pubmed-78385442021-01-28 Impact of Long-Term Organic and Mineral Fertilization on Rhizosphere Metabolites, Root–Microbial Interactions and Plant Health of Lettuce Windisch, Saskia Sommermann, Loreen Babin, Doreen Chowdhury, Soumitra Paul Grosch, Rita Moradtalab, Narges Walker, Frank Höglinger, Birgit El-Hasan, Abbas Armbruster, Wolfgang Nesme, Joseph Sørensen, Søren Johannes Schellenberg, Ingo Geistlinger, Jörg Smalla, Kornelia Rothballer, Michael Ludewig, Uwe Neumann, Günter Front Microbiol Microbiology Fertilization management can affect plant performance and soil microbiota, involving still poorly understood rhizosphere interactions. We hypothesized that fertilization practice exerts specific effects on rhizodeposition with consequences for recruitment of rhizosphere microbiota and plant performance. To address this hypothesis, we conducted a minirhizotron experiment using lettuce as model plant and field soils with contrasting properties from two long-term field experiments (HUB-LTE: loamy sand, DOK-LTE: silty loam) with organic and mineral fertilization history. Increased relative abundance of plant-beneficial arbuscular mycorrhizal fungi and fungal pathotrophs were characteristic of the rhizospheres in the organically managed soils (HU-org; BIODYN2). Accordingly, defense-related genes were systemically expressed in shoot tissues of the respective plants. As a site-specific effect, high relative occurrence of the fungal lettuce pathogen Olpidium sp. (76–90%) was recorded in the rhizosphere, both under long-term organic and mineral fertilization at the DOK-LTE site, likely supporting Olpidium infection due to a lower water drainage potential compared to the sandy HUB-LTE soils. However, plant growth depressions and Olpidium infection were exclusively recorded in the BIODYN2 soil with organic fertilization history. This was associated with a drastic (87–97%) reduction in rhizosphere abundance of potentially plant-beneficial microbiota (Pseudomonadaceae, Mortierella elongata) and reduced concentrations of the antifungal root exudate benzoate, known to be increased in presence of Pseudomonas spp. In contrast, high relative abundance of Pseudomonadaceae (Gammaproteobacteria) in the rhizosphere of plants grown in soils with long-term mineral fertilization (61–74%) coincided with high rhizosphere concentrations of chemotactic dicarboxylates (succinate, malate) and a high C (sugar)/N (amino acid) ratio, known to support the growth of Gammaproteobacteria. This was related with generally lower systemic expression of plant defense genes as compared with organic fertilization history. Our results suggest a complex network of belowground interactions among root exudates, site-specific factors and rhizosphere microbiota, modulating the impact of fertilization management with consequences for plant health and performance. Frontiers Media S.A. 2021-01-13 /pmc/articles/PMC7838544/ /pubmed/33519736 http://dx.doi.org/10.3389/fmicb.2020.597745 Text en Copyright © 2021 Windisch, Sommermann, Babin, Chowdhury, Grosch, Moradtalab, Walker, Höglinger, El-Hasan, Armbruster, Nesme, Sørensen, Schellenberg, Geistlinger, Smalla, Rothballer, Ludewig and Neumann. http://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 Microbiology
Windisch, Saskia
Sommermann, Loreen
Babin, Doreen
Chowdhury, Soumitra Paul
Grosch, Rita
Moradtalab, Narges
Walker, Frank
Höglinger, Birgit
El-Hasan, Abbas
Armbruster, Wolfgang
Nesme, Joseph
Sørensen, Søren Johannes
Schellenberg, Ingo
Geistlinger, Jörg
Smalla, Kornelia
Rothballer, Michael
Ludewig, Uwe
Neumann, Günter
Impact of Long-Term Organic and Mineral Fertilization on Rhizosphere Metabolites, Root–Microbial Interactions and Plant Health of Lettuce
title Impact of Long-Term Organic and Mineral Fertilization on Rhizosphere Metabolites, Root–Microbial Interactions and Plant Health of Lettuce
title_full Impact of Long-Term Organic and Mineral Fertilization on Rhizosphere Metabolites, Root–Microbial Interactions and Plant Health of Lettuce
title_fullStr Impact of Long-Term Organic and Mineral Fertilization on Rhizosphere Metabolites, Root–Microbial Interactions and Plant Health of Lettuce
title_full_unstemmed Impact of Long-Term Organic and Mineral Fertilization on Rhizosphere Metabolites, Root–Microbial Interactions and Plant Health of Lettuce
title_short Impact of Long-Term Organic and Mineral Fertilization on Rhizosphere Metabolites, Root–Microbial Interactions and Plant Health of Lettuce
title_sort impact of long-term organic and mineral fertilization on rhizosphere metabolites, root–microbial interactions and plant health of lettuce
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7838544/
https://www.ncbi.nlm.nih.gov/pubmed/33519736
http://dx.doi.org/10.3389/fmicb.2020.597745
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