Expression pattern changes of three homeologs in chemokine activity enhance antiviral response to herpesvirus infection in a newly synthesized alloheptaploid

Allopolyploids often exhibit enhanced resistance to pathogen stresses. However, our understanding about the patterns that allopolyploids modify homeolog expression upon pathogen invasion remains limited. Since 2012, a disease caused by herpesvirus ( Ca HV) has posed a severe threat to Carassius auratus aquaculture. Therefore, the synthesis of novel allopolyploids with enhanced resistance has become one of significant priorities for its aquaculture. In this study, we first synthesized and then established a gynogenetic Carassius alloheptaploid clone ( Ca A7n). It possesses approximately 158 chromosomes of C. gibelio and 24 haploid chromosomes of M. amblycephala . Ca HV challenge experiments showed that Ca A7n inherited high resistance from its paternal M. amblycephalus , exhibiting a 100% survival rate after Ca HV infection. Subsequently, we revealed distinct transcriptional responses among Ca A7n and its parents to Ca HV infection and identified two key modules. The egiengenes in the module that positively correlated with Ca A7n resistance were mainly enriched in chemokine activity GO terms. Finally, we described a profound expression alteration of three homeologs in Ca A7n, including additive and non-additive expression patterns. After Ca HV infection, three homeologs mainly involved in chemokine activity changed their expression patterns in Ca A7n. Moreover, homeologs derived from M. amblycephala associated with chemokine activity, which showed altered expression levels, may enhance the antiviral immune response of Ca A7n. This study not only establishes Ca A7n as a promising Ca HV-resistant candidate for aquaculture but also elucidates how allopolyploids reconfigure parental homeolog expression networks to enhance antiviral defenses, advancing our understanding of allopolyploid adaptation mechanisms under pathogenic pressure.