Evaluation of Phenolic Root Exudates as Stimulants of Saptrophic Fungi in the Rhizosphere

The rhizosphere microbial community of crop plants in intensively managed arable soils is strongly dominated by bacteria, especially in the initial stages of plant development. In order to establish more diverse and balanced rhizosphere microbiomes, as seen for wild plants, crop variety selection co...

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Main Authors: Anna Clocchiatti, S. Emilia Hannula, Marlies van den Berg, Maria P. J. Hundscheid, Wietse de Boer
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-04-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.644046/full
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author Anna Clocchiatti
Anna Clocchiatti
S. Emilia Hannula
Marlies van den Berg
Maria P. J. Hundscheid
Wietse de Boer
Wietse de Boer
author_facet Anna Clocchiatti
Anna Clocchiatti
S. Emilia Hannula
Marlies van den Berg
Maria P. J. Hundscheid
Wietse de Boer
Wietse de Boer
author_sort Anna Clocchiatti
collection DOAJ
description The rhizosphere microbial community of crop plants in intensively managed arable soils is strongly dominated by bacteria, especially in the initial stages of plant development. In order to establish more diverse and balanced rhizosphere microbiomes, as seen for wild plants, crop variety selection could be based on their ability to promote growth of saprotrophic fungi in the rhizosphere. We hypothesized that this can be achieved by increasing the exudation of phenolic acids, as generally higher fungal abundance is observed in environments with phenolic-rich inputs, such as exudates of older plants and litter leachates. To test this, a rhizosphere simulation microcosm was designed to establish gradual diffusion of root exudate metabolites from sterile sand into arable soil. With this system, we tested the fungus-stimulating effect of eight phenolic acids alone or in combination with primary root metabolites. Ergosterol-based fungal biomass measurements revealed that most phenolic acids did not increase fungal abundance in the arable soil layer. These results were supported by comparison of fungal biomass in the rhizosphere of wild type Arabidopsis thaliana plants and mutants with altered phenolic acid metabolism. Salicylic acid was the only phenolic acid that stimulated a higher fungal biomass in the arable soil layer of microcosms, but only when combined with a background of primary root metabolites. However, such effect on rhizosphere fungi was not confirmed for a salicylic acid-impaired A. thaliana mutant. For three phenolic acid treatments (chlorogenic acid, salicylic acid, vanillic acid) fungal and bacterial community compositions were analyzed using amplicon sequencing. Despite having little effect on fungal biomass, phenolic acids combined with primary metabolites promoted a higher relative abundance of soil-borne fungi with the ability to invade plant roots (Fusarium, Trichoderma and Fusicolla spp.) in the simulated rhizosphere. Bacterial community composition was also affected by these phenolic acids. Although this study indicates that phenolic acids do not increase fungal biomass in the rhizosphere, we highlight a potential role of phenolic acids as attractants for root-colonizing fungi.
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spelling doaj.art-b26bbccaa7164af9b4cc3f766819a7902022-12-21T23:00:44ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-04-011210.3389/fmicb.2021.644046644046Evaluation of Phenolic Root Exudates as Stimulants of Saptrophic Fungi in the RhizosphereAnna Clocchiatti0Anna Clocchiatti1S. Emilia Hannula2Marlies van den Berg3Maria P. J. Hundscheid4Wietse de Boer5Wietse de Boer6Netherlands Institute of Ecology (NIOO-KNAW), Wageningen, NetherlandsSoil Biology Group, Wageningen University, Wageningen, NetherlandsNetherlands Institute of Ecology (NIOO-KNAW), Wageningen, NetherlandsNetherlands Institute of Ecology (NIOO-KNAW), Wageningen, NetherlandsNetherlands Institute of Ecology (NIOO-KNAW), Wageningen, NetherlandsNetherlands Institute of Ecology (NIOO-KNAW), Wageningen, NetherlandsSoil Biology Group, Wageningen University, Wageningen, NetherlandsThe rhizosphere microbial community of crop plants in intensively managed arable soils is strongly dominated by bacteria, especially in the initial stages of plant development. In order to establish more diverse and balanced rhizosphere microbiomes, as seen for wild plants, crop variety selection could be based on their ability to promote growth of saprotrophic fungi in the rhizosphere. We hypothesized that this can be achieved by increasing the exudation of phenolic acids, as generally higher fungal abundance is observed in environments with phenolic-rich inputs, such as exudates of older plants and litter leachates. To test this, a rhizosphere simulation microcosm was designed to establish gradual diffusion of root exudate metabolites from sterile sand into arable soil. With this system, we tested the fungus-stimulating effect of eight phenolic acids alone or in combination with primary root metabolites. Ergosterol-based fungal biomass measurements revealed that most phenolic acids did not increase fungal abundance in the arable soil layer. These results were supported by comparison of fungal biomass in the rhizosphere of wild type Arabidopsis thaliana plants and mutants with altered phenolic acid metabolism. Salicylic acid was the only phenolic acid that stimulated a higher fungal biomass in the arable soil layer of microcosms, but only when combined with a background of primary root metabolites. However, such effect on rhizosphere fungi was not confirmed for a salicylic acid-impaired A. thaliana mutant. For three phenolic acid treatments (chlorogenic acid, salicylic acid, vanillic acid) fungal and bacterial community compositions were analyzed using amplicon sequencing. Despite having little effect on fungal biomass, phenolic acids combined with primary metabolites promoted a higher relative abundance of soil-borne fungi with the ability to invade plant roots (Fusarium, Trichoderma and Fusicolla spp.) in the simulated rhizosphere. Bacterial community composition was also affected by these phenolic acids. Although this study indicates that phenolic acids do not increase fungal biomass in the rhizosphere, we highlight a potential role of phenolic acids as attractants for root-colonizing fungi.https://www.frontiersin.org/articles/10.3389/fmicb.2021.644046/fullphenolic acidsroot exudatessaprotrophic fungifungal biomassfungal communityTrichoderma
spellingShingle Anna Clocchiatti
Anna Clocchiatti
S. Emilia Hannula
Marlies van den Berg
Maria P. J. Hundscheid
Wietse de Boer
Wietse de Boer
Evaluation of Phenolic Root Exudates as Stimulants of Saptrophic Fungi in the Rhizosphere
Frontiers in Microbiology
phenolic acids
root exudates
saprotrophic fungi
fungal biomass
fungal community
Trichoderma
title Evaluation of Phenolic Root Exudates as Stimulants of Saptrophic Fungi in the Rhizosphere
title_full Evaluation of Phenolic Root Exudates as Stimulants of Saptrophic Fungi in the Rhizosphere
title_fullStr Evaluation of Phenolic Root Exudates as Stimulants of Saptrophic Fungi in the Rhizosphere
title_full_unstemmed Evaluation of Phenolic Root Exudates as Stimulants of Saptrophic Fungi in the Rhizosphere
title_short Evaluation of Phenolic Root Exudates as Stimulants of Saptrophic Fungi in the Rhizosphere
title_sort evaluation of phenolic root exudates as stimulants of saptrophic fungi in the rhizosphere
topic phenolic acids
root exudates
saprotrophic fungi
fungal biomass
fungal community
Trichoderma
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.644046/full
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