Species diversity of Cladosporium in Citrus and the genetic mechanisms for C. cladosporioides complex to adapt broad host plants

Abstract Cladosporium represents one of the most common fungal groups on plants and has been reported as a core microbiome of several plants. Some species are important for agriculture because they are pathogens causing diseases in some economically significant crops. In this study, a systematic investigation of Cladosporium associated with citrus in China was carried out. In total, 502 isolates representing 16 species belonging to three species complexes were isolated from fruits, leaves and twigs of 20 common citrus varieties collected across 10 major citrus-producing provinces in China. Among them, C. cladosporioides complex species is predominant, accounting for 95% of all isolates. The distribution of Cladosporium species on citrus was found to be associated with symptoms and geography. Pathogenicity tests confirmed that C. tenuissimum , C. pseudocladosporioides , C. anthropophilum and C. xanthochromaticum are pathogenic to fruits of several Citrus varieties. We sequenced 21 genomes and combined 21 Cladosporium genomes from database to produce a high-confidence phylogeny and confirmed the C. sphaerospermum complex is polyphyletic. Pangenome analysis reveals different functional preferences of specific genes between species complexes. Interestingly, C. cladosporioides complex species have significantly higher number of encoding genes involved in carbohydrate-active enzymes, plant cell wall-degrading enzymes, and secreted peptidases compared with other species complexes. Conversely, effector proteins involved in host immune suppression are notably scarce across all Cladosporium species, including the C. cladosporioides complex. Additionally, several members of the C. cladosporioides complex encodes some secondary metabolites with antimicrobial activities. Together, our study not only provides insights into the diversity and distribution of Cladosporium on citrus and their genomic evolution and adaptation, but also explains the reasons for the dominance of the C. cladosporioides complex on plants.