Stage-specific transcriptomic and DNA methylation responses to triploidy in European sea bass embryos and larvae.

backgroundPolyploidy, the condition of having more than two chromosome sets, is relatively common in plants but rare in animals, largely due to reproductive challenges associated with altered chromosome numbers. In fish, however, polyploidy occurs naturally in several species, and triploidy can be artificially induced in aquaculture to optimize growth and suppress sexual maturation. Induced triploidy results in sterility, especially in females, while remarkably preserving a largely conserved somatic gene expression program and adult phenotype, suggesting mechanisms of gene dosage compensation. However, the epigenetic mechanisms regulating gene expression following triploidy induction remain poorly understood. This knowledge gap is especially evident during early embryogenesis, a critical but understudied developmental window. To address this, we investigated the effects of induced triploidization in the European sea bass on gene expression and DNA methylation at two developmental stages: 90% epiboly and hatching, known as highly and poorly sensitive to triploidy induction, respectively. This approach also aimed to provide a global view into the molecular mechanisms that contribute to triploids' resilience.

resultsWe identified 1,204 and 712 differentially expressed genes (DEGs) when comparing triploids against diploids at epiboly and hatching, respectively. However, while DEGs were mainly downregulated at epiboly, they were upregulated at hatching. Enrichment analysis revealed 32 enriched pathways at epiboly and two at hatching. Global DNA methylation levels were unaffected by triploidy. However, ~ 30,000 differentially methylated cytosines (DMCs) were identified, with ~ 50% of them mapping to the promoter region, exons and introns. Approximately 4,200 genes contained at least one DMC, and 211 and 76 genes were both differentially expressed and methylated (DEMGs) at epiboly and hatching, respectively.

conclusionsThese results reveal a distinct stage-specific transcriptome response to triploidy induction, while the limited number of DEMGs suggests regulatory mechanisms beyond DNA methylation contribute to maintaining gene expression homeostasis in triploids. Such mechanisms might help explain, at least in part, the moderate reduction in survival observed compared with diploids.