Rainbow trout (Oncorhynchus mykiss) is a species of cold-water fish with important economic values, widely cultivated worldwide. However, the outbreak of infectious hematopoietic necrosis virus (IHNV) caused the large-scale death of rainbow trout and seriously restricted the development of the trout farming industry. In this study, the changes of immune parameters in different periods (6-, 12-, 24-, 48-, 72-, 96-, 120-, and 144 h post-
infection (hpi)), transcriptome profiles of 48 hpi (T48G) compared to control (C48G), and key immune-related genes expression patterns were measured in rainbow trout gill following IHNV challenge through biochemical methods,
RNA sequencing (
RNA-seq), and quantitative real-time polymerase chain reaction (qRT-PCR). The results showed that
alkaline phosphatase (AKP),
acid phosphatase (ACP), total
superoxide dismutase (T-SOD),
alanine aminotransferase (ALT), and
aspartate aminotransferase (AST) activities, as well as
lysozyme (LZM) and
malonaldehyde (MDA) content decreased and then increased during
infection, and remained at a high level after 48 hpi (P < 0.05), whereas
catalase (CAT) activity showed a significant peak at 48 hpi (P < 0.05). The
mRNA and
miRNA analysis identified 4343 differentially expressed genes (DEGs) and 11 differentially expressed
miRNAs (DEMs), and numerous immune-related DEGs involved in the
Toll-like receptor signaling pathway, apoptosis, DNA replication, p53 signaling, RIG-I-like receptor signaling pathway, and
NOD-like receptor signaling pathway and expression were significantly up-regulated in T48Gm group, including tlr3, tlr7, tlr8,
traf3, ifih1, trim25, dhx58, ddh58, hsp90a.1, nlrc3, nlrc5, socs3, irf3, irf7, casp7, mx1, and vig2. The integrated analysis identified several important
miRNAs (ola-miR-27d-3p_R+5, gmo-miR-124-3-5p, ssa-miR-301a-5p_L+2, and ssa-miR-146d-3p) that targeted key immune-related DEGs. Expression analysis showed that tlr3, tlr7,
traf3, ifih1, dhx58, hap90a.1, irf3, irf7, and mx1 genes increased and then decreased during
infection, and peaked at 72 hpi (P < 0.05). However, trim25 expression peaked at 96 hpi (P < 0.05). This study contributes to understanding immune response of rainbow trout against IHNV
infection, and provides new insights into the immune regulation mechanisms and
disease resistance breeding studies.