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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.

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