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Comparative Transcriptome Analysis of Key Genes and Pathways Activated in Response to Fat Deposition in Two Sheep Breeds With Distinct Tail Phenotype.

ABSTRACT: Fat tail in sheep presents a valuable energy reserve that has historically facilitated adaptation to harsh environments. However, in modern intensive and semi-intensive sheep industry systems, breeds with leaner tails are more desirable. In the present study, RNA sequencing (RNA-Seq) was applied to determine the transcriptome profiles of tail fat tissues in two Chinese sheep breeds, fat-rumped Altay sheep and thin-tailed Xinjiang fine wool (XFW) sheep, with extreme fat tail phenotype difference. Then the differentially expressed genes (DEGs) and their sequence variations were further analyzed. In total, 21,527 genes were detected, among which 3,965 displayed significant expression variations in tail fat tissues of the two sheep breeds (P < 0.05), including 707 upregulated and 3,258 downregulated genes. Gene Ontology (GO) analysis disclosed that 198 DEGs were related to fat metabolism. In Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis, the majority of DEGs were significantly enriched in "adipocytokine signaling," "PPAR signaling," and "metabolic pathways" (P < 0.05); moreover, some genes were involved in multiple pathways. Among the 198 DEGs, 22 genes were markedly up- or downregulated in tail fat tissue of Altay sheep, indicating that these genes might be closely related to the fat tail trait of this breed. A total of 41,724 and 42,193 SNPs were detected in the transcriptomic data of tail fat tissues obtained from Altay and XFW sheep, respectively. The distribution of seven SNPs in the coding regions of the 22 candidate genes was further investigated in populations of three sheep breeds with distinct tail phenotypes. In particular, the g.18167532T/C (Oar_v3.1) mutation of the ATP-binding cassette transporter A1 (ABCA1) gene and g.57036072G/T (Oar_v3.1) mutation of the solute carrier family 27 member 2 (SLC27A2) gene showed significantly different distributions and were closely associated with tail phenotype (P < 0.05). The present study provides transcriptomic evidence explaining the differences in fat- and thin-tailed sheep breeds and reveals numerous DEGs and SNPs associated with tail phenotype. Our data provide a valuable theoretical basis for selection of lean-tailed sheep breeds.

SUBMITTER: Zhang W

PROVIDER: S-EPMC8060577 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:The level of fat deposition in carcass is a crucial factor influencing meat quality. Guangling Large-Tailed (GLT) and Small-Tailed Han (STH) sheep are important local Chinese fat-tailed breeds that show distinct patterns of fat depots. To gain a better understanding of fat deposition, transcriptome profiles were determined by RNA-sequencing of perirenal, subcutaneous, and tail fat tissues from both the sheep breeds. The common highly expressed genes (co-genes) in all the six tissues, and the genes that were differentially expressed (DE genes) between these two breeds in the corresponding tissues were analyzed. RESULTS:Approximately 47 million clean reads were obtained for each sample, and a total of 17,267 genes were annotated. Of the 47 highly expressed co-genes, FABP4, ADIPOQ, FABP5, and CD36 were the four most highly transcribed genes among all the known genes related to adipose deposition. FHC, FHC-pseudogene, and ZC3H10 were also highly expressed genes and could, thus, have roles in fat deposition. A total of 2091, 4233, and 4131 DE genes were identified in the perirenal, subcutaneous, and tail fat tissues between the GLT and STH breeds, respectively. Gene Ontology (GO) analysis showed that some DE genes were associated with adipose metabolism. Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis revealed that PPAR signaling pathway and ECM-receptor interaction were specifically enriched. Four genes, namely LOC101102230, PLTP, C1QTNF7, and OLR1 were up-regulated and two genes, SCD and UCP-1, were down-regulated in all the tested tissues of STH. Among the genes involved in ECM-receptor interaction, the genes encoding collagens, laminins, and integrins were quite different depending on the depots or the breeds. In STH, genes such as LAMB3, RELN, TNXB, and ITGA8, were identified to be up regulated and LAMB4 was observed to be down regulated. CONCLUSIONS:This study unravels the complex transcriptome profiles in sheep fat tissues, highlighting the candidate genes involved in fat deposition. Further studies are needed to investigate the roles of the candidate genes in fat deposition and in determining the meat quality of sheep.

Project description:The fat tail is a phenotype that divides indigenous Iranian sheep genetic resources into two major groups. The objective of the present study is to refine the map location of candidate regions associated with fat deposition, obtained via two separate whole genome scans contrasting thin and fat tail breeds, and to determine the nature of the selection occurring in these regions using a hitchhiking approach. Zel (thin tail) and Lori-Bakhtiari (fat tail) breed samples that had previously been run on the Illumina Ovine 50 k BeadChip, were genotyped with a denser set of SNPs in the three candidate regions using a Sequenom Mass ARRAY platform. Statistical tests were then performed using different and complementary methods based on either site frequency (FST and Median homozygosity) or haplotype (iHS and XP-EHH). The results from candidate regions on chromosome 5 and X revealed clear evidence of selection with the derived haplotypes that was consistent with selection to near fixation for the haplotypes affecting fat tail size in the fat tail breed. An analysis of the candidate region on chromosome 7 indicated that selection differentiated the beneficial alleles between breeds and homozygosity has increased in the thin tail breed which also had the ancestral haplotype. These results enabled us to confirm the signature of selection in these regions and refine the critical intervals from 113 kb, 201 kb, and 2831 kb to 28 kb, 142 kb, and 1006 kb on chromosome 5, 7, and X respectively. These regions contain several genes associated with fat metabolism or developmental processes consisting of TCF7 and PPP2CA (OAR5), PTGDR and NID2 (OAR7), AR, EBP, CACNA1F, HSD17B10,SLC35A2, BMP15, WDR13, and RBM3 (OAR X), and each of which could potentially be the actual target of selection. The study of core haplotypes alleles in our regions of interest also supported the hypothesis that the first domesticated sheep were thin tailed, and that fat tail animals were developed later. Overall, our results provide a comprehensive assessment of how and where selection has affected the patterns of variation in candidate regions associated with fat deposition in thin and fat tail sheep breeds.

Project description:An essential tissue involved in the development and regulation of lipid metabolism in animals is adipose tissue. The “fat-tail” can supply energy for sheep during migration and winter when a low amount of dry matter intake is available. Tail fat content affects meat quality and varies significantly among the different breeds of sheep. Ghezel (fat-tailed) and Zel (thin-tailed) are two important local Iranian sheep breeds that show different patterns of fat storage. The current study presents the transcriptome characterization of tail fat using RNA-sequencing in order to get a better comprehension of the molecular mechanism of lipid storage in the two sheep breeds. The results of sequencing were analyzed with bioinformatics methods, including differentially expressed genes (DEGs) identification, functional enrichment analysis, structural classification of proteins, protein–protein interaction (PPI), network analysis and module analysis. The results revealed a total of332 DEGs between the Zel and Ghezel breed, with78 up-regulated and 254 down-regulated DEGs in the Zel breed. Identification of differential genes showed that some DEGs, such as IL-6, LIPG, SAA1, SOCS3 and HIF-1α, with the largest fold change had close association with lipid deposition. Also, important lipid storage genes such as FASN and SCPEP1 had high levels of expression. Furthermore, functional enrichment analysis revealed some pathways associated with fat deposition, such as “Fatty acid metabolism”, “Fatty acid biosynthesis” and“HIF-1 signaling pathway”. In addition, structural classification of proteins showed major DEGs in transcription factor classes such as JUNB, NR4A3, FOSL1, MAFF, NR4A1, CREB3L1 and ATF3 were up-regulated in the Zel breed. IL-6, JUNB, and related DEGs were up-regulated in the PPI network.HMGCS1, SUCLA2 and STT3B and related DEGs were down-regulated in the PPI network and had high topology scores as hub genes. This implies the DEGs of these modules are important candidate genes for tail fat metabolism and, therefore, can be further studied.

Project description:Hu sheep and Tibetan sheep are two commonly raised local sheep breeds in China, and they have different morphological characteristics, such as tail type and adaptability to extreme environments. A fat tail in sheep is the main adipose depot in sheep, whereas the liver is an important organ for fat metabolism, with the uptake, esterification, oxidation, and secretion of fatty acids (FAs). Meanwhile, adaptations to high-altitude and arid environments also affect liver metabolism. Therefore, in this study, RNA-sequencing (RNA-seq) technology was used to characterize the difference in liver fat metabolism between Hu sheep and Tibetan sheep. We identified 1179 differentially expressed genes (DEGs) (Q-value < 0.05) between the two sheep breeds, including 25 fat-metabolism-related genes. Through Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis, 16 pathways were significantly enriched (Q-value < 0.05), such as the proteasome, glutamatergic synapse, and oxidative phosphorylation pathways. In particular, one of these pathways was enriched to be associated with fat metabolism, namely the thermogenesis pathway, to which fat-metabolism-related genes such as ACSL1, ACSL4, ACSL5, CPT1A, CPT1C, SLC25A20, and FGF21 were enriched. Then, the expression levels of ACSL1, CPT1A, and FGF21 were verified in mRNA and protein levels via qRT-PCR and Western blot analysis between the two sheep breeds. The results showed that the mRNA and protein expression levels of these three genes were higher in the livers of Tibetan sheep than those of Hu sheep. The above genes are mainly related to FAs oxidation, involved in regulating the oxidation of liver FAs. So, this study suggested that Tibetan sheep liver has a greater FAs oxidation level than Hu sheep liver. In addition, the significant enrichment of fat-metabolism-related genes in the thermogenesis pathway appears to be related to plateau-adaptive thermogenesis in Tibetan sheep, which may indicate that liver- and fat-metabolism-related genes have an impact on adaptive thermogenesis.

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Comparative Transcriptome Analysis of Key Genes and Pathways Activated in Response to Fat Deposition in Two Sheep Breeds With Distinct Tail Phenotype.

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