Abstract
BACKGROUND: Soil microbiomes are important for plant growth and health. The objectives of this study were to characterize boxwood root-zone microbial community and understand their associations with plant disease resistance and other horticultural traits. Soil samples were collected from four cultivars with three distinct boxwood blight tolerance at two geographically distant nursery locations in May, August, and November of 2021. Bacterial and fungal communities were characterized through DNA metabarcoding. RESULTS: The dominant bacteria in the boxwood root-zone soil included Bacillus and several unknown genera of the order Gaiellales and families Xanthobacteraceae and Gemmatimonadaceae; the dominant fungi included Clonostachys, an unknown genus, Solicoccozyma, and Fusarium. Ceratobasidium, Hyaloscypha, and Sistotrema were also the dominant genera within the presumptive mycorrhizal fungi (PMF) group. Fungal community structure was distinct among cultivars with different blight tolerance in May and August, but the divergence of the bacterial community structure was only significant in the August samples. Community composition-wise, greater numbers of genera differed in abundance between the intermediate and the susceptible cultivars. Moreover, cross-kingdom network analysis showed a more connected network constructed from the intermediate cultivars and identified more hub taxa as module connectors compared with the other two cultivars. Some of the hub taxa, including bacterial genera Gaiella, Streptomyces, and Sphingomonas, and fungal genera Solicoccozyma and Pseudonectria were also among the 27 bacterial and 6 fungal core genera identified from all samples across four cultivars, two locations, and three seasons. Further, Volutella and Pseudonectria were negatively associated with 10 bacterial genera and all identified PMF-PMF connections were positive across all networks. CONCLUSIONS: Boxwood root-zone soil harbored diverse plant-beneficial microbes, including PMFs. Fungal community and microbial network connectivity also differed among the cultivars, suggesting the regulatory roles of plant phenotype and genotype in fungi recruitment and microbial interactions. Several keystone taxa were identified and may be crucial in maintaining the structure and communication within the boxwood root-zone microbiome. The negative associations between bacteria and Volutella/Pseudonectria provide a new insight into managing the rise of the boxwood Volutella blight. Together, this study offers several leads to enhancing plant resilience to disease and environmental stress. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-025-08094-1.