Allele-specific expression reveals the phenotypic differences between thin- and fat-tailed sheep

Abstract

Background: The thin-tailed sheep breeds from Europe and the fat-tailed sheep breeds from China exhibit distinct phenotypic differences in fat deposition and meat production traits. However, the molecular mechanisms underlying gene expression related to these phenotypic differences are not well understood. Allele-specific expression (ASE) refers to the significant imbalance of expression levels of two parental alleles. Characterization of such events in F1 hybrid offspring generated from these two groups of sheep breeds can minimize the external factors influencing gene expression and reveal the variants with a cis -regulatory effect on gene expression. The aim of the present study was to investigate the genetic factors that influence different fat-deposition and meat production traits between thin- and fat-tailed sheep.Results: Fifteen F1 hybrids were generated from crosses between Texel and Kazakh sheep as the representative phenotypes of thin- and fat-tailed breeds, respectively. Totally, 33 whole genomes from F1 individuals and their parents were sequenced with an average depth of ~17.21× coverage per sample. ASE analysis results from 70 RNA-seq samples of adipose and skeleton muscle tissues showed 128 ASE candidate genes were related to the function of fat deposition and meat production traits. A genome-wide scan of selective sweeps was also conducted between these two groups of sheep breeds in an effort to identify genomic regions related to fat deposition and meat production, respectively. We detected signatures of selection in ASE genes associated with fat deposition (e.g., PDGFD ) and meat production traits (e.g., LRCC2 ). Further analysis suggested that PDGFD and LRCC2 genes were speculated to be causative genes for fat deposition and meat production traits in sheep, respectively. Furthermore, AMPK signaling pathway was significantly enriched in ASE genes related to fatty acid biosynthesis in both adipose and skeleton muscle tissues, while PPAR signaling pathway was significantly enriched in ASE genes related to lipid metabolism in adipose tissue. Conclusions: Our finding illustrates that the expression of identified ASE genes could potentially lead to the differences in traits of fat deposition and meat production between thin- and fat-tailed sheep. Keywords: allele-specific expression, phenotypic difference, thin- and fat-tailed sheep, whole-genome sequencing, transcriptome

Trends towards revealing the genetic architecture of sheep tail patterning: Promising genes and investigatory pathways

“…With advancements in genomic research technologies, the understanding of genetic bases underlying evolutionally and agriculturally valuable traits has drastically increased (Kijas et al 2012;Jiang et al 2014;Lv et al 2014Lv et al , 2015Yang et al 2016;Zhao et al 2017;Naval-Sanchez et al 2018;Pan et al 2018;Hu et al 2019;Cao et al 2021). Since 2012, various genomic-based studies have been conducted to understand the genetic basis and genomic architecture of sheep tails and to find the specific causal genomic variant(s) contributing to sheep tail patternmaking (Moradi et al 2012;Moioli et al 2015;Wei et al 2015;Pan et al 2019;Dong et al 2020b;Li et al 2020b;Shao et al 2020;Luo et al 2021) (Fig. 2).…”

“…Later, Shao et␣al . (2020) highlighted seven allele‐specific expression (ASE) SNPs from eight adipose tissue samples (four from tail fat and four from subcutaneous fat) in the PDGFD gene through ASE analysis (Shao et␣al . 2020).…”

“…Figure 2 A brief overview on genomic outcomes, including proposed potential genes generated from investigations on the sheep tail phenotype (Moradi et al 2012;Moioli et al 2015;Wei et al 2015;Zhu et al 2016Zhu et al , 2021Xu et al 2017;Yuan et al 2017;Zhi et al 2018;Ahbara et al 2019;Manzari et al 2019;Mastrangelo et al 2019aMastrangelo et al , 2019bPan et al 2019;Zhang et al 2019;Dong et al 2020b;Li et al 2020b;Shao et al 2020;Zhao et al 2020;Baazaoui et al 2021;Luo et al 2021;Tao et al 2021;Moradi et al 2021). Repeatedly revealed genes are marked in colors.…”

“…Li et al (2020b) proposed a distinct genotype pattern in the promoter region of the PDGFD gene that could be related to the differences in the sheep tail phenotypic patterns. By contrast, Shao et al (2020) suggested the possibility of SNPs located within the 3 0 -UTR region to likely be bind ports for regulatory microRNAs that influence gene expression. Additionally, this study also highlighted the potential of a distinct genotype pattern in the upstream region of the PDGFD gene, harboring regulatory elements such as enhancers, which affect the gene expression between fat-tailed and thin-tailed sheep breeds (Shao et al 2020).…”

“…By contrast, Shao et al (2020) suggested the possibility of SNPs located within the 3 0 -UTR region to likely be bind ports for regulatory microRNAs that influence gene expression. Additionally, this study also highlighted the potential of a distinct genotype pattern in the upstream region of the PDGFD gene, harboring regulatory elements such as enhancers, which affect the gene expression between fat-tailed and thin-tailed sheep breeds (Shao et al 2020). To date, the genomic investigations that have been performed to elucidate the differences in sheep tail patterning could determine the PDGFD gene as a predominant gene responsible for these phenotypic differences.…”