The bark latent fungus Botryosphaeria dothidea exacerbates branch dieback following the infection with Verticillium dahliae

Verticillium wilt, caused by the soilborne fungus Verticillium dahliae, has resulted in high mortality of Cotinus coggygria (smoke tree) in China. Symptoms of this disease are complex, many infected smoke trees exhibit wilting or dieback on some branches but no other branches. Whether other microbial taxa act synergistically to contribute to symptom development is unknown. Here, we investigated the microbial community assembly features associated with different branches of smoke trees with or without Verticillium wilt symptoms and established linkages between symptomatic branches and putative keystone taxa. Amplicon data analyses revealed that V. dahliae significantly affected the microbiota structure within tree branches. Microbial network connectivity indicated that Verticillium wilt destabilized the network, and fungal communities were more sensitive to Verticillium wilt than the bacterial communities. Based on taxonomic level information, the fungus Botryosphaeria dothidea was significantly enriched in diseased branches and positively correlated with the abundance of V. dahliae. Through microbial isolations, pathogen co-inoculations, histopathological assays, and RNA-seq analyses, the results indicated that plants infected with V. dahliae showed significantly increased susceptibility to B. dothidea and downregulated expression of defense-related genes. Overall, the results revealed that Verticillium wilt provokes changes in the structure of the smoke tree microbiome and that these changes likely influence symptom development in some but not all tree branches. The synergistic interplay between the commensal fungus B. dothidea and the soil-borne fungus V. dahliae promotes wilt progression in smoke trees, offering new insights into developing effective control strategies through fungicides plus enhancing host vigor.