Apple Genotypes and Soil Properties Shape the Soil Microbiome and Influence the Plant Response to Replant Disease-Affected Soil

Apple replant disease (ARD) is a problem in apple tree and fruit production worldwide, and its etiology is not fully understood. This study aimed to evaluate the tolerance of six apple genotypes, including the susceptible rootstock M.26; three potentially tolerant rootstocks, EMR.2, G.202, and G.935; and two wild-type accessions, Malus spectabilis MAL0130 and Malus sargentii MAL0739 in ARD soils from six sites. Using a greenhouse biotest, plants were grown for 56 days in ARD or the respective γ-irradiated soil. No genotype showed a consistent lack of growth reduction in all ARD soils, indicating that no universal tolerance existed within the tested set of genotypes. Three genotypes (M.26, MAL0130, and MAL0739) were selected for analyses of ARD indicator gene expression and phytoalexin contents in roots as measures of ARD response. Biphenyl synthase 3 expression and phytoalexin content strongly correlated with highest levels observed in roots of the susceptible rootstock M.26. MAL0739 showed the lowest response, which was not consistently reflected in improved plant growth across all soils. Analysis of the bacterial and fungal communities in three root-affected ARD soils revealed soil- and genotype-specific differences. Bacterial alpha diversity was higher in MAL0739 compared with M.26, whereas beta diversity was mainly shaped by the soil. Significant enrichment of Nectria was observed for M.26 grown in one ARD soil. Phytoalexin contents and potentially plant-beneficial microbial taxa correlated negatively. Our findings highlight that ARD tolerance in apple genotypes is linked to the soil microbiome and other soil properties, indicating the need for an integrated approach to managing ARD.