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Mycoplasma synoviae (MS), an important avian pathogen, can cause chronic respiratory disease, eggshell apex abnormalities, infectious synovitis, and arthritis in avian species, leading serious economic losses in the global poultry industry. To date, studies have shown significant different transcript profiles using various chicken cells after MS infection. However, in vitro cell models cannot fully represent the complex in vivo regulations after adventitious infection. The objective of this study was to explore the nature of the host-pathogen interaction during MS infection. The tracheal and spleen tissues of chickens were collected at d 0, 1, 3, and 5 postinoculation, and samples were analyzed for differential gene expression using Illumina RNA sequencing. A lot of significantly differentially expressed genes (DEGs) were observed in this analysis, and 861 DEGs were observed in trachea tissues and 753 DEGs were observed in spleen samples. Many of DEGs in trachea tissues participate in a variety of cellular activities, especially cellular metabolism. Immune-related DEGs were mainly enriched at d 3, and 5 postinfection in trachea tissues. While, DEGs in spleen tissues were significantly and mainly enriched into immune-related pathways. The results of this study show the direct interactions between MS and the chicken trachea and spleen for the first time. Early dysregulation of tissue-wide gene expression as observed here set the stage for persistent infection of MS. [ABSTRACT FROM AUTHOR]