Dietary α-Linolenic Acid Enrichment Is Associated with p38 Mapk/FoxO1-Related Signaling and Improved Fillet Quality in Nile Tilapia (Oreochromis niloticus)

Farmed tilapia fillets are often perceived as having poor eating quality due to their soft texture and low content of n-3 long-chain polyunsaturated fatty acids (LC-PUFA). Dietary α-linolenic acid (ALA) has been proposed as a potential strategy to improve these characteristics, although the underlying mechanism remains unclear. Juvenile Nile tilapia (Oreochromis niloticus) were fed either a soybean-oil-based diet (D1, 0.58% ALA) or a soybean-oil/linseed-oil diet (D2, 1.35% ALA) for 8 weeks, followed by analyses of muscle quality, transcriptomic profiles, and cell responses. The results demonstrated that growth performance and muscle proximate composition did not differ significantly between treatments, whereas condition factor was significantly higher in the D2 group. Compared with D1, D2 was associated with an increase in n-3 PUFA proportion from 8.05% to 23.71% and a 1.97-fold increase in LC-PUFA, along with reductions in n-6 PUFA (−24.3%) and saturated fatty acids (−11.6%). Six texture attributes measured, namely hardness, chewiness, gumminess, springiness, resilience and cohesiveness were higher in D2 fish, whereas adhesiveness did not differ significantly between treatments. D2 fish also exhibited higher muscle fiber density and a greater proportion of small-diameter fibers. Transcriptomic analysis identified 207 differentially expressed genes (24 upregulated and 183 downregulated) enriched in pathways related to cardiac muscle contraction, adrenergic signaling, lipid metabolism and FoxO signaling. Network analysis grouped the sarcomeric/myogenic and atrophy-related genes (mstn, foxo1, p38 mapk, mkk4) into two inversely correlated modules, with foxo1 emerging as the most highly connected gene. Muscle qPCR confirmed the up-regulation of myod and myf5 and the down-regulation of mstn, p38 mapk and foxo1 in D2 fish. In myoblasts, ALA increased cell viability and myogenic factor expression while suppressing p38 mapk and foxo1, and these effects were attenuated by hesperetin. Overall, the ALA-enriched dietary lipid formulation was associated with a more favorable muscle fatty acid profile and texture characteristics in Nile tilapia. The cell-based findings further suggest the potential involvement of p38 Mapk/FoxO1-related signaling, although its causal role requires further validation.