Comparative transcriptome analysis reveals distinct immune response in different ploidy cyprinid caudal fin cells following SVCV infection

Abstract

Triploid fish (3n = 150) exhibit enhanced disease resistance compared to their parents—red crucian carp (♀, 2n = 100) and allotetraploid (♂, 4n = 200). To elucidate the innate immunity of triploid hybrid, a comparative transcriptomic analysis was carried out to elucidate the molecular events during spring viraemia of carp virus (SVCV) infection in caudal fin cell from the red crucian carp, triploid hybrid and allotetraploid, denoted as G2n, G3n, and G4n, respectively. KEGG enrichment analysis indicated that SVCV may alter the host cell's metabolic profiles post-infection, and the ECM-mediated adhesion plaque signaling pathway may facilitate the virus's recognition and infection processes. Distinct signaling regulation mechanisms in response to SVCV infection were observed across different ploidy levels. In G2n, immune-related pathways such as the TNF signaling pathway and Toll-like receptor signaling pathway were activated. The downregulation of immune related gene, such as MHC I, may indicate viral strategies to evade detection by the immune system through inhibited antigen presentation in diploid fish. Apoptosis-related processes including the Apoptosis, Phagosome, Rap1 signaling pathway, and Hippo signaling pathway were significantly enriched in G4n, indicating SVCV hijack the host autophagy and apoptosis to improve their replication and spreading. The outcomes of the comparative analysis demonstrate that, in G3n, robust protective barriers against SVCV invasion were established through the downregulation of MMP9, mTOR, p53, and NCAM, alongside the upregulation of MHC I, CLDN, and CAV 1-mediated interactions. This coordinated multi-gene response might be a key factor contributing to the enhanced resistance of triploid fish. The findings underscore the distinct signal regulation of different ploidy cyprinid fish in response to SVCV infection, providing valuable reference data for the prevention and treatment of SVCV.