Transcriptomic analyses revealed common tailed and perirenal adipose differentially expressed genes in four Chinese indigenous sheep breeds

Highlights

• Differentially expressed genes (DEGs) in three tissues from Hu sheep were detected.

• Common DEGs in perirenal and tail adipose tissue across four breeds were revealed.

• Several common DEGs may affect the unsaturated fatty acid content in tail fat.

ABSTRACT

Fat deposition and distribution in different body sites are associated with livestock productivity. In some sheep breeds, fat is excessively accumulated around the tail region, which is regarded as the fat-tail phenotype. Though some plausible genes or genomic regions associated with the fat-tail phenotype were identified, further validation of them in different individuals and breeds is still required. In this study, we implemented differential expression analysis using RNA-seq data in longissimus dorsi muscle tissue (MUT), perirenal adipose tissue (PAT) and tail adipose tissue (TAT) of Hu sheep, which is a representative of short fat-tailed sheep. The result identified 1336, 427 and 665 differentially expressed genes (DEGs) in MUT, PAT and TAT of Hu sheep respectively. Of those, 600 DEGs and 336 DEGs showed unique expression in TAT and PAT, respectively. In addition, integrated analyses of our data with published data from small-tailed Han sheep, Guangling large-tailed sheep and Tan sheep found 9 DEGs in PAT and 13 DEGs in TAT of Hu sheep have similar expression patterns in the remaining three sheep breeds. Among 9 DEGs in PAT, WT1, TCF21, PPFIBP1 and WNT10B may have important roles in perirenal adipose formation. Among 13 DEGs in TAT, PKD2L1 and MST1 may play significant roles in the maintenance of unsaturated fatty acid content in TAT. Five genes that were previously reported to be correlated with tailed fat deposition were further validated in current study, including CITED1, HOTAIR_2, HOTAIR_3, HOXC12 and HOXC13. Furthermore, we also investigated the expression pattern of 42 candidate genes identified by selection signature analysis or genome wide association analysis from published studies. Two of them were found to be highly expressed in TAT, including PPP1CA and PEX6. Our findings identify candidate genes for tail fat deposition across different breeds and pave a solid foundation for studying the regulation of fat deposition in sheep in the future.

Introduction

Fat depositions in different body sites are of significant interest to select desirable livestock for breeding and production. In some sheep breeds, fat is excessively accumulated around the tail region, which is regarded as the fat-tail phenotype. According to the length and shape of the tail, fat-tailed sheep can be further divided into short fat-tailed, long fat-tailed, and fat-rumped types (Mohapatra and Shinde, 2018). Different from other mammals, the unique distribution of sheep fat, i.e. the fat-tail phenotype, has attracted increasing interest. On one hand, fat tail has lost its commercial value because customers preferred lower-fat meat. On the other hand, protecting this special trait may have a potential role for the future breeding for adaptation to a harsh environment. Hence, it is important for sheep industry to identify the candidate genes associated with tail fat deposition and further understand the genetic mechanism underlying this process.

Previously, some candidate genes or genomic regions associated with the fat tail characteristic were identified by contrasting divergent phenotypes or via association with tailed phenotype (Moradi et al., 2012; Moioli et al., 2015; Wei et al., 2015; Zhu et al., 2016; Xu et al., 2017; Yuan et al., 2017; Li et al., 2018; Ma et al., 2018b; Mastrangelo et al., 2018; Zhi et al., 2018; Ahbara et al., 2019). These studies laid the foundation for studying the formation of sheep tail fat. However, the causal genes for such a phenotype remains unclear. Exploring differentially expressed genes (DEGs) in different tissues is a way to identify important candidate genes because the variation in the gene expression across tissues is attributable to their functionality. Recently, researchers identified some DEGs or specifically expressed genes by comparing adipose tissues from several body sites in Tan sheep, Guangling large-tailed sheep, and small-tailed Han sheep (Kang et al., 2017; Li et al., 2018). Animal species and breeds can differ in their characteristics related to adipose tissue deposition (Hausman et al., 2014). The short fat-tailed Hu sheep is one of the most widely raised indigenous sheep breeds in China known for its high fecundity (Yue, 1996). Its gene expression pattern in different adipose tissue types has not been thoroughly investigated.

The evidence from previous studies suggest some common genes associated with the tail fat phenotype are shared across different breeds (Moioli et al., 2015; Yuan et al., 2017; Mastrangelo et al., 2018). Our hypothesis for this study was that an integrative study combining the results of RNA-seq in different breeds could reveal strong candidate genes for the complex fat tailed phenotype. In the current study, we used RNA-seq technology to identify DEGs in three different tissues, namely tail adipose tissue (TAT), perirenal adipose tissue (PAT) and longissimus dorsi muscle tissue (MUT) from Hu Sheep. In addition, we incorporated published RNA-seq data (Guangling large-tailed sheep and small-tailed Han sheep, Table 1) and summary data (mean reads per kilobase per million mapped reads, RPKM) of DEGs’ in Tan sheep to investigate the common DEGs across different breeds (Kang et al., 2017; Li et al., 2018). Further, we also investigated the expression pattern of 42 candidate genes in Hu sheep, small-tailed Han sheep and Guangling large-tailed sheep, which were identified by selection signature analysis or genome wide association analysis from the published literature.