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

Shangquan Gan,Wei Zhang,Xinhua Wang,Juanjuan Wang,Mengsi Xu,Lei Gao,Shiyin Wang,Jingquan Yang

doi:10.3389/fgene.2021.639030

Shangquan Gan, Wei Zhang + Show 6 more

Open Access

https://doi.org/10.3389/fgene.2021.639030

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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.

Highlights

Fat tail is a valuable trait that helps sheep (Ovis aries) adapt to harsh conditions, such as extremely cold winters, food shortages, and drought seasons
We identified 245 and 187 DEGs enriched in the MAPK and insulin signaling pathways, respectively, indicating potential roles of these mechanisms in tail/rump fat metabolism of Altay and XFW sheep
We focused on the 22 candidate genes related to tail fat metabolism, which led to the identification of 13 SNPs in the coding regions of nine genes, among which 12 induced amino acid alterations (Table 3)

Summary

Introduction

Fat tail is a valuable trait that helps sheep (Ovis aries) adapt to harsh conditions, such as extremely cold winters, food shortages, and drought seasons. According to archaeological and genomic findings, modern sheep breeds were domesticated at the Fertile Crescent region of Iraq about 9,000 years ago (Zeder, 1999; Handley et al, 2007; Chessa et al, 2009). Similar to their Asian mouflon ancestor, modern sheep breeds were thin tailed at the early stages. Elucidation of the key genes that regulate the deposition and decomposition of tail fat in sheep and the molecular mechanisms controlling fat metabolism would greatly accelerate the breeding course of lean-tailed sheep and production of more healthy mutton to the market

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