Transgenerational Immune Priming (TGIP) and Its Potential Association with EGR1 in Penaeus vannamei.

Acute hepatopancreatic necrosis disease (AHPND) caused by Vibrio parahaemolyticus remains one of the most serious bacterial diseases affecting Penaeus vannamei aquaculture. Immune priming has recently emerged as a promising strategy for enhancing disease resistance in aquatic animals. However, the molecular basis of immune priming and its potential effects on offspring remain poorly understood. In this study, UV-inactivated V. parahaemolyticus (V160807) was used to induce immune priming in P. vannamei. Primed F0 female shrimp were subsequently bred to obtain F1 offspring, and disease resistance, histopathology, cellular immunity, humoral immunity, transcriptome profiles, and DNA methylation patterns were evaluated. Both the F0 and F1 generations exhibited higher survival rates, lower bacterial loads, enhanced hemocyte-bacteria binding capacity, and stronger immune-related enzyme activities following bacterial challenge. Transcriptome analysis revealed significant enrichment of genes associated with pathogen recognition, melanization, and immune signaling pathways. In particular, pattern recognition receptor (PRR)-related genes, including CLEC4G and DSCAML1, were markedly upregulated. Whole-genome bisulfite sequencing (WGBS) showed that histone H3 genes were hypomethylated, whereas ATP synthase-related genes displayed hypermethylation. These changes were accompanied by suppression of several energy metabolism pathways. Integrated transcriptomic and WGBS analyses identified EGR1 as a candidate regulatory gene. In F0 shrimp, EGR1 exhibited promoter and gene-body hypermethylation accompanied by reduced expression. Similar methylation changes were detected at the EGR1 locus in F1 offspring, including a conserved 61 bp hypermethylated region within the promoter. Pyrosequencing and RT-qPCR were further used to evaluate the methylation and expression patterns of EGR1. These findings demonstrate that prior exposure to UV-inactivated V. parahaemolyticus induces immune priming in F0 shrimp and is associated with enhanced disease resistance and immune response in F1 offspring. The EGR1 DNA methylation and gene expression changes may contribute to the establishment of maternal TGIP.