Colletotrichum gloeosporioides Swiftly Manipulates the Transcriptional Regulation in Citrus sinensis During the Early Infection Stage

<i>Citrus</i> spp. represent an economically important fruit tree crop worldwide. However, molecular mechanisms underlying the interaction between citrus and the <i>Colletotrichum gloeosporioides</i> remain largely unexplored. In this study, we analyzed the physiological and transcriptomic changes in <i>Citrus sinensis</i> at different stages of incubation with <i>C. gloeosporioides</i>. The results indicated that <i>C. gloeosporioides</i> infection rapidly triggered necrosis in the epicarp of <i>C. sinensis</i> fruits, decreased the total flavonoid contents, and suppressed the activity of catalase, peroxidase, and superoxide dismutase enzymes. Upon inoculation with <i>C. gloeosporioides</i>, there were 4600 differentially expressed genes (DEGs) with 1754 down-regulated and 2846 up-regulated after six hours, while there were only 580 DEGs with 185 down-regulated and 395 up-regulated between six and twelve-hours post-inoculation. Gene Ontology and the Kyoto Encyclopedia of Genes and Genomes enrichment analysis indicated that the DEGs, which exhibited consistent up-regulation, were associated with metabolic processes and stress responses. Through Weighted Gene Co-Expression Network Analysis, 11 key genes have been identified that could potentially play a role in the transcriptional regulation of this process, including the transcription factor bHLH189. Furthermore, the infection of <i>C. gloeosporioides</i> had a notable effect on both the flavonoid metabolism and the metabolic pathways related to reactive oxygen species. Our findings help to understand the interaction between citrus and <i>C. gloeosporioides</i> and unveil how new insights into how <i>C. gloeosporioides</i> circumvents citrus defense mechanisms.