Dataset Information

Gene expression profiling of trout muscle during flesh quality recovery following spawning.

ABSTRACT:

Background

Sexual maturation causes loss of fish muscle mass and deterioration of fillet quality attributes that prevent market success. We recently showed that fillet yield and flesh quality recover in female trout after spawning. To gain insight into the molecular mechanisms regulating flesh quality recovery, we used an Agilent-based microarray platform to conduct a large-scale time course analysis of gene expression in female trout white muscle from spawning to 33 weeks post-spawning.

Results

In sharp contrast to the situation at spawning, muscle transcriptome of female trout at 33 weeks after spawning was highly similar to that of female trout of the same cohort that did not spawn, which is consistent with the post-spawning flesh quality recovery. Large-scale time course analysis of gene expression in trout muscle during flesh quality recovery following spawning led to the identification of approximately 3340 unique differentially expressed genes that segregated into four major clusters with distinct temporal expression profiles and functional categories. The first cluster contained approximately 1350 genes with high expression at spawning and downregulation after spawning and was enriched with genes linked to mitochondrial ATP synthesis, fatty acid catabolism and proteolysis. A second cluster of approximately 540 genes with transient upregulation 2 to 8 weeks after spawning was enriched with genes involved in transcription, RNA processing, translation, ribosome biogenesis and protein folding. A third cluster containing approximately 300 genes upregulated 4 to 13 weeks after spawning was enriched with genes encoding ribosomal subunits or regulating protein folding. Finally, a fourth cluster that contained approximately 940 genes with upregulation 8 to 24 weeks after spawning, was dominated by genes encoding myofibrillar proteins and extracellular matrix components and genes involved in glycolysis.

Conclusion

Overall, our study indicates that white muscle tissue restoration and flesh quality recovery after spawning are associated with transcriptional changes promoting anaerobic ATP production, muscle fibre hypertrophic growth and extracellular matrix remodelling. The generation of the first database of genes associated with post-spawning muscle recovery may provide insights into the molecular and cellular mechanisms controlling muscle yield and fillet quality in fish and provide a useful list of potential genetic markers for these traits.

SUBMITTER: Ahongo YD

PROVIDER: S-EPMC8725336 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Sexual maturation causes loss of fish muscle mass and deterioration of fillet quality attributes that prevent market purpose. We recently showed that fillet yield and flesh quality are recovered in female trout after spawning. To gain insights into the molecular mechanisms regulating flesh quality recovery we conducted a time-course analysis of large-scale gene expression in trout muscle from spawning to 33 weeks post-spawning. Using an Agilent-based microarray plate-form, we identified about 5500 unique genes that were differentially expressed during the post-spawning period. These genes segregated into four major clusters with distinct temporal expression profile and functional categories. A first cluster containing around 2000 genes down-regulated after 4 weeks after spawning was enriched in genes linked to mitochondrial ATP synthesis, fatty acid catabolism and proteolysis. A second cluster comprising about 1200 genes with early and transient induction between 2 to 8 weeks post-spawning was enriched in genes involved in RNA processing, translation, ribosome biogenesis and protein folding. A third cluster containing about 700 genes up-regulated from 4 weeks post-spawning onwards was enriched in genes encoding ribosomal subunits or regulating translation and cell cycle. At last a fourth cluster which contained about 1000 genes with late up-regulation from 13 weeks post- spawning onwards, was dominated by genes encoding myofibrillar proteins and matricial components and genes involved in glycolysis. On the whole our study indicates that muscle tissue restoration and flesh quality recovery occurring after spawning is mainly associated with anaerobic ATP production, muscle fibre hypertrophic growth, fatty acid metabolism and extracellular matrix remodelling. The generation of the first database of genes associated with post-spawning muscle recovery will allow future mechanistic studies and facilitate identification of genetic markers for fish muscle yield and quality traits.

Project description:BackgroundGrowth in fishes is regulated via many environmental and physiological factors and is shaped by the genetic background of each individual. Previous microarray studies of salmonid growth have examined fish experiencing either muscle wastage or accelerated growth patterns following refeeding, or the influence of growth hormone and transgenesis. This study determines the gene expression profiles of genetically unmanipulated large and small fish from a domesticated salmonid strain reared on a typical feeding regime. Gene expression profiles of white muscle and liver from rainbow trout (Oncorhynchus mykiss) from two seasonal spawning groups (September and December lots) within a single strain were examined when the fish were 15 months of age to assess the influence of season (late fall vs. onset of spring) and body size (large vs. small).ResultsAlthough IGFBP1 gene expression was up-regulated in the livers of small fish in both seasonal lots, few expression differences were detected in the liver overall. Faster growing Dec. fish showed a greater number of differences in white muscle expression compared to Sept. fish. Significant differences in the GO Generic Level 3 categories 'response to external stimulus', 'establishment of localization', and 'response to stress' were detected in white muscle tissue between large and small fish. Larger fish showed up-regulation of cytoskeletal component genes while many genes related to myofibril components of muscle tissue were up-regulated in small fish. Most of the genes up-regulated in large fish within the 'response to stress' category are involved in immunity while in small fish most of these gene functions are related to apoptosis.ConclusionsA higher proportion of genes in white muscle compared to liver showed similar patterns of up- or down-regulation within the same size class across seasons supporting their utility as biomarkers for growth in rainbow trout. Differences between large and small Sept. fish in the 'response to stress' and 'response to external stimulus' categories for white muscle tissue, suggests that smaller fish have a greater inability to handle stress compared to the large fish. Sampling season had a significant impact on the expression of genes related to the growth process in rainbow trout.

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