Reduced microbial potential for the degradation of phenolic compounds in the rhizosphere of apple plantlets grown in soils affected by replant disease

Abstract Background Apple replant disease (ARD) is a syndrome that occurs in areas where apple plants or closely related species have been previously cultivated. Even though ARD is a well-known phenomenon, which has been observed in different regions worldwide and occurs independent of the soil type...

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Main Authors: Viviane Radl, Jana Barbro Winkler, Susanne Kublik, Luhua Yang, Traud Winkelmann, Gisle Vestergaard, Peter Schröder, Michael Schloter
Format: Article
Language:English
Published: BMC 2019-11-01
Series:Environmental Microbiome
Subjects:
Online Access:http://link.springer.com/article/10.1186/s40793-019-0346-2
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author Viviane Radl
Jana Barbro Winkler
Susanne Kublik
Luhua Yang
Traud Winkelmann
Gisle Vestergaard
Peter Schröder
Michael Schloter
author_facet Viviane Radl
Jana Barbro Winkler
Susanne Kublik
Luhua Yang
Traud Winkelmann
Gisle Vestergaard
Peter Schröder
Michael Schloter
author_sort Viviane Radl
collection DOAJ
description Abstract Background Apple replant disease (ARD) is a syndrome that occurs in areas where apple plants or closely related species have been previously cultivated. Even though ARD is a well-known phenomenon, which has been observed in different regions worldwide and occurs independent of the soil type, its causes still remain unclear. Results As expected, the biomass of plants grown in replant soil was significantly lower compared to those grown in control (virgin) soil. A shotgun metagenome analysis showed a clear differentiation between the rhizosphere and bulk soil compartments independent from the soil used. However, significant differences associated with apple replant disease were only observed in the rhizosphere compartment, for which we detected changes in the abundance of major bacterial genera. Interestingly, reads assigned to Actinobacteria were significantly reduced in relative abundance in rhizosphere samples of the soil affected by replant disease. Even though reads assigned to pathogenic fungi were detected, their relative abundance was low and did not differ significantly between the two different soils. Differences in microbiome structure also resulted in shifts in functional pattern. We observed an increase in genes related to stress sensing in the rhizosphere of soils affected by replant disease, whereas genes linked to nutrient sensing and uptake dominated in control soils. Moreover, we observed a lower abundance of genes coding for enzymes which trigger the degradation of aromatic compounds in rhizosphere of soils affected by replant disease, which is probably connected with higher concentration of phenolic compounds, generally associated with disease progression. Conclusions Our study shows, for the first time, how apple replanting affects soil functioning by altering the soil microbiome. Particularly, the decrease in the abundance of genes which code for enzymes catalyzing the degradation of aromatic compounds, observed in the rhizosphere of plants grown in soil affected by apple replant disease, is of interest. Apple rootstocks are known to synthetize many phenolic compounds, including defense related phytoalexins, which have been considered for long to be connected with the emergence of replant disease. The knowledge gained in this study might help to develop targeted strategies to overcome or at least reduce the effects of ARD symptoms.
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spelling doaj.art-b715c8e44b4e429caa24d19e147711a62022-12-22T02:22:43ZengBMCEnvironmental Microbiome2524-63722019-11-0114111210.1186/s40793-019-0346-2Reduced microbial potential for the degradation of phenolic compounds in the rhizosphere of apple plantlets grown in soils affected by replant diseaseViviane Radl0Jana Barbro Winkler1Susanne Kublik2Luhua Yang3Traud Winkelmann4Gisle Vestergaard5Peter Schröder6Michael Schloter7Research Unit Comparative Microbiome Analysis, Helmholtz Zentrum MünchenResearch Unit Environmental Simulations, Helmholtz Zentrum MünchenResearch Unit Comparative Microbiome Analysis, Helmholtz Zentrum MünchenResearch Unit Comparative Microbiome Analysis, Helmholtz Zentrum MünchenWoody Plant and Propagation Physiology Section, Institute of Horticultural Production Systems, Leibniz Universität HannoverResearch Unit Comparative Microbiome Analysis, Helmholtz Zentrum MünchenResearch Unit Comparative Microbiome Analysis, Helmholtz Zentrum MünchenResearch Unit Comparative Microbiome Analysis, Helmholtz Zentrum MünchenAbstract Background Apple replant disease (ARD) is a syndrome that occurs in areas where apple plants or closely related species have been previously cultivated. Even though ARD is a well-known phenomenon, which has been observed in different regions worldwide and occurs independent of the soil type, its causes still remain unclear. Results As expected, the biomass of plants grown in replant soil was significantly lower compared to those grown in control (virgin) soil. A shotgun metagenome analysis showed a clear differentiation between the rhizosphere and bulk soil compartments independent from the soil used. However, significant differences associated with apple replant disease were only observed in the rhizosphere compartment, for which we detected changes in the abundance of major bacterial genera. Interestingly, reads assigned to Actinobacteria were significantly reduced in relative abundance in rhizosphere samples of the soil affected by replant disease. Even though reads assigned to pathogenic fungi were detected, their relative abundance was low and did not differ significantly between the two different soils. Differences in microbiome structure also resulted in shifts in functional pattern. We observed an increase in genes related to stress sensing in the rhizosphere of soils affected by replant disease, whereas genes linked to nutrient sensing and uptake dominated in control soils. Moreover, we observed a lower abundance of genes coding for enzymes which trigger the degradation of aromatic compounds in rhizosphere of soils affected by replant disease, which is probably connected with higher concentration of phenolic compounds, generally associated with disease progression. Conclusions Our study shows, for the first time, how apple replanting affects soil functioning by altering the soil microbiome. Particularly, the decrease in the abundance of genes which code for enzymes catalyzing the degradation of aromatic compounds, observed in the rhizosphere of plants grown in soil affected by apple replant disease, is of interest. Apple rootstocks are known to synthetize many phenolic compounds, including defense related phytoalexins, which have been considered for long to be connected with the emergence of replant disease. The knowledge gained in this study might help to develop targeted strategies to overcome or at least reduce the effects of ARD symptoms.http://link.springer.com/article/10.1186/s40793-019-0346-2MetagenomeApple replant diseaseMalus domesticaMicrobiomeRhizosphere
spellingShingle Viviane Radl
Jana Barbro Winkler
Susanne Kublik
Luhua Yang
Traud Winkelmann
Gisle Vestergaard
Peter Schröder
Michael Schloter
Reduced microbial potential for the degradation of phenolic compounds in the rhizosphere of apple plantlets grown in soils affected by replant disease
Environmental Microbiome
Metagenome
Apple replant disease
Malus domestica
Microbiome
Rhizosphere
title Reduced microbial potential for the degradation of phenolic compounds in the rhizosphere of apple plantlets grown in soils affected by replant disease
title_full Reduced microbial potential for the degradation of phenolic compounds in the rhizosphere of apple plantlets grown in soils affected by replant disease
title_fullStr Reduced microbial potential for the degradation of phenolic compounds in the rhizosphere of apple plantlets grown in soils affected by replant disease
title_full_unstemmed Reduced microbial potential for the degradation of phenolic compounds in the rhizosphere of apple plantlets grown in soils affected by replant disease
title_short Reduced microbial potential for the degradation of phenolic compounds in the rhizosphere of apple plantlets grown in soils affected by replant disease
title_sort reduced microbial potential for the degradation of phenolic compounds in the rhizosphere of apple plantlets grown in soils affected by replant disease
topic Metagenome
Apple replant disease
Malus domestica
Microbiome
Rhizosphere
url http://link.springer.com/article/10.1186/s40793-019-0346-2
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