Canker Disease Intensifies Cross-Kingdom Microbial Interactions in the Endophytic Microbiota of Citrus Phyllosphere

Plant disease is an important factor that affects the plant microbiome. However, for many plant–pathogen–microbiome interactions, the influences are unknown. Citrus, comprising abundant varieties of mandarin, sweet orange, pomelo, and lemon, is widely cultivated in different production areas in China. Most of these varieties are vulnerable to citrus canker, which is caused by Xanthomonas spp. In this study, asymptomatic and cankered leaves from asymptomatic and canker-infected trees, respectively, were collected from 17 orchards in six citrus production areas and their endophytic microbiomes were compared. The effects of canker on the microbial community richness and diversity were dependent on whether the interaction type was intrakingdom (for bacteria, positive) and interkingdom (for fungi, negative), respectively. The negative effects of canker on the fungal communities might be affected by the strong correlation between Xanthomonas and Fusarium/ Gibberella species. The occurrence of canker significantly affected the composition and structure of both the endophytic fungal and bacterial communities, and altered the dominant genera of each community. In addition, canker occurrence intensified the cross-kingdom microbial interaction network, in which species of Enterobacter, Xanthomonas, Pseudomonas, and Pantoea were detected with increased roles in the network and responsible for the predominant functional genes involved in nutritional metabolism, the bacterial secretion system, and biotin metabolism. The results provide insights into the responses of the endophytic microbiome to citrus canker disease.