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. 2023 May 15:10:1150996.
doi: 10.3389/fvets.2023.1150996. eCollection 2023.

Transcriptome analysis of perirenal fat from Spanish Assaf suckling lamb carcasses showing different levels of kidney knob and channel fat

María Alonso-García  1 , Aroa Suárez-Vega  1 , Pablo A S Fonseca  1 , Héctor Marina  1 , Rocío Pelayo  1 , Javier Mateo  2 , Juan-José Arranz  1 , Beatriz Gutiérrez-Gil  1
Affiliations

Transcriptome analysis of perirenal fat from Spanish Assaf suckling lamb carcasses showing different levels of kidney knob and channel fat

María Alonso-García et al. Front Vet Sci. .

Abstract

Introduction: Suckling lamb meat is highly appreciated in European Mediterranean countries because of its mild flavor and soft texture. In suckling lamb carcasses, perirenal and pelvic fat depots account for a large fraction of carcass fat accumulation, and their proportions are used as an indicator of carcass quality.

Material and methods: This study aimed to characterize the genetic mechanisms that regulate fat deposition in suckling lambs by evaluating the transcriptomic differences between Spanish Assaf lambs with significantly different proportions of kidney knob and channel fat (KKCF) depots in their carcasses (4 High-KKCF lambs vs. 4 Low-KKCF lambs).

Results: The analyzed fat tissue showed overall dominant expression of white adipose tissue gene markers, although due to the young age of the animals (17-36 days), the expression of some brown adipose tissue gene markers (e.g., UCP1, CIDEA) was still identified. The transcriptomic comparison between the High-KKCF and Low-KKCF groups revealed a total of 80 differentially expressed genes (DEGs). The enrichment analysis of the 49 DEGs with increased expression levels in the Low-KKCF lambs identified significant terms linked to the biosynthesis of lipids and thermogenesis, which may be related to the higher expression of the UCP1 gene in this group. In contrast, the enrichment analysis of the 31 DEGs with increased expression in the High-KKCF lambs highlighted angiogenesis as a key biological process supported by the higher expression of some genes, such as VEGF-A and THBS1, which encode a major angiogenic factor and a large adhesive extracellular matrix glycoprotein, respectively.

Discussion: The increased expression of sestrins, which are negative regulators of the mTOR complex, suggests that the preadipocyte differentiation stage is being inhibited in the High-KKCF group in favor of adipose tissue expansion, in which vasculogenesis is an essential process. All of these results suggest that the fat depots of the High-KKCF animals are in a later stage of development than those of the Low-KKCF lambs. Further genomic studies based on larger sample sizes and complementary analyses, such as the identification of polymorphisms in the DEGs, should be designed to confirm these results and achieve a deeper understanding of the genetic mechanisms underlying fat deposition in suckling lambs.

Keywords: RNA-seq; carcass traits; fat deposition; gene expression; lamb; perirenal fat.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Gene expression distribution of the perirenal fat transcriptomes of the two groups of Assaf suckling lams considered in this study, High-KKCF (in blue) and Low-KKCF (in orange). The bar graph displays the expression intensity distribution of the transcripts identified in the datasets analyzed. The number of genes is represented on the Y-axis, whereas the X-axis represents the different expression level groups considered for the classification, in fragments per kilobase per million mapped (FPKMs): 0.01–5, 5–50, 50–100, 100–150, and more than 150 FPKMs. The number of genes within each category and group is indicated at the top of each bar.
Figure 2
Figure 2
Bar chart showing the gene expression levels, in FPKMs, of different genetic markers reported in the literature for the different types of adipose tissue; brown (BAT), beige (BeAT), and white (WAT) adipose tissue, for the two groups of perirenal fat transcriptomes of suckling lambs analyzed: High-KKCF group (blue) and Low-KKCF group (orange). Each of the bars indicates the mean expression of the genes on the X-axis and the gray lines of each bar indicate the standard deviation of expression for each gene in the two groups of samples compared. The horizontal red line indicates the expression threshold level of >150 FPKMs considered to define the genes belonging to the core representative genes (CRG) of the suckling lamb fat transcriptome.
Figure 3
Figure 3
Graphical representation of the results of the enrichment analysis performed with clusterProfiler for the differentially expressed genes (DEGs) in the Low-KKCF group (LowKKCF-DEGs). (A) Network of enriched terms and LowKKCF-DEGs that are related to these terms. The orange color scale for the genes indicates their corresponding Log2FoldChange value. (B) Dendrogram of the significant enriched terms identified for the LowKKCF-DEGs showing their clustering according to their biological relationship. The size of the circle associated to each term is proportional to the number of genes supporting it. The color intensity of the circle depends on the significance level (p value adjusted according to the FDR correction for multiple testing).
Figure 4
Figure 4
Graphical representation of the results of the enrichment analysis performed with clusterProfiler for the differentially expressed genes (DEGs) in the High-KKCF group (HighKKCF-DEGs). (A) Network of enriched terms and HighKKCF-DEGs that are related to these terms. The orange color scale for the genes indicates their corresponding Log2FoldChange value. (B) Dendrogram of the significant enriched terms identified for the HighKKCF-DEGs showing their clustering according to their biological relationship. The size of the circle associated to each term is proportional to the number of genes supporting it. The color intensity of the circle depends on the significance level (p value adjusted according to the FDR correction for multiple testing).
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