Relationship between root-endophytic microbial communities and replant disease in specialized apple growing areas in Europe

•Apple replant disease was evaluated over three European countries.•A growth test was performed on replanted fallow and gamma ray-treated soil samples.•Replant disease resulted mainly from biotic factors.•Cylindrocarpon-like and Pythium populations were negatively correlated with plant growth.•Changes of root-endophyte fungal communities seem to reduce replant disease. Apple replant disorders are one of the causes of the downward trend of land planted with apple orchards in Central Europe. A specific transnational survey was thus conducted on apple root associated microorganisms, aimed at increasing the knowledge regarding crop management to counteract this tendency. Soil health was evaluated using a bioassay test with root cuttings of the clonal M9 rootstock, one of the most commonly used rootstocks in Europe. Plant growth response in replant, fallow and gamma ray-sterilized soil was evaluated using soil samples taken from nine orchards selected (three per country) from specialized apple growing areas of Germany, Austria and Italy. Plant growth significantly differed between treatments but not between countries. Root endophytic fungi were confirmed as one of the main components of growth reduction, while endophytic nematodes (Pratylenchus sp.) were not. The large set of quantitative and qualitative data of root endophytic fungi allowed to clarify that Cylindrocarpon-like fungi (Ilyonectria spp. and Thelonectria sp.) had a major pathogenic role in the three countries, while Pythium spp. prevailed as pathogen only in German orchards. Gamma ray-sterilized soil resulted in a more-than-proportional increase of plant growth (42% and 31% respectively vs. replant and fallow) as compared to that observed between fallow and replant soil (18%). This best performance in gamma ray-sterilized soil, in addition to the lowest root colonization by Cylindrocarpon-like fungi in this treatment, appeared to be due to the different composition of fungal communities as compared to two other treatments (fallow and replant soil), which instead were highly similar to each other. This difference was due to a shift of community composition toward Fusarium and binucleate Rhizoctonia, which prevailed in sterilized soil.