Integrated Multi-Tissue Transcriptome Profiling Characterizes the Genetic Basis and Biomarkers Affecting Reproduction in Sheep (Ovis aries)

Zaixia Liu; Shaoyin Fu; Xiaolong He; Lingli Dai; Xuewen Liu; Narisu; Caixia Shi; Mingjuan Gu; Yu Wang; Manda; Lili Guo; Yanchun Bao; Baiyinbatu; Chencheng Chang; Yongbin Liu; Wenguang Zhang

doi:10.3390/genes14101881

Integrated Multi-Tissue Transcriptome Profiling Characterizes the Genetic Basis and Biomarkers Affecting Reproduction in Sheep (Ovis aries)

Genes (Basel). 2023 Sep 27;14(10):1881. doi: 10.3390/genes14101881.

Authors

Zaixia Liu^{1

2}, Shaoyin Fu³, Xiaolong He³, Lingli Dai^{1

2

4}, Xuewen Liu⁵, Narisu^{1

2}, Caixia Shi¹, Mingjuan Gu^{1

2}, Yu Wang⁶, Manda¹, Lili Guo^{1

2

7}, Yanchun Bao^{1

2}, Baiyinbatu^{1

2}, Chencheng Chang^{1

2}, Yongbin Liu⁷, Wenguang Zhang^{1

2

8}

Affiliations

¹ College of Animal Science, Inner Mongolia Agricultural University, Hohhot 010018, China.
² Inner Mongolia Engineering Research Center of Genomic Big Data for Agriculture, Hohhot 010018, China.
³ Institute of Animal Husbandry, Inner Mongolia Academy of Agricultural and Animal Husbandry Sciences, Hohhot 010031, China.
⁴ Veterinary Research Institute, Inner Mongolia Academy of Agricultural and Animal Husbandry Sciences, Hohhot 010031, China.
⁵ Animal Husbandry and Bioengineering, College of Agronomy, Xing'an Vocational and Technical College, Ulanhot 137400, China.
⁶ College of Veterinary Medicine, Inner Mongolia Agricultural University, Hohhot 010018, China.
⁷ School of Life Science, Inner Mongolia University, Hohhot 010021, China.
⁸ College of Life Science, Inner Mongolia Agricultural University, Hohhot 010018, China.

Abstract

The heritability of litter size in sheep is low and controlled by multiple genes, but the research on its related genes is not sufficient. Here, to explore the expression pattern of multi-tissue genes in Chinese native sheep, we selected 10 tissues of the three adult ewes with the highest estimated breeding value in the early study of the prolific Xinggao sheep population. The global gene expression analysis showed that the ovary, uterus, and hypothalamus expressed the most genes. Using the Uniform Manifold Approximation and Projection (UMAP) cluster analysis, these samples were clustered into eight clusters. The functional enrichment analysis showed that the genes expressed in the spleen, uterus, and ovary were significantly enriched in the Ataxia Telangiectasia Mutated Protein (ATM) signaling pathway, and most genes in the liver, spleen, and ovary were enriched in the immune response pathway. Moreover, we focus on the expression genes of the hypothalamic-pituitary-ovarian axis (HPO) and found that 11,016 genes were co-expressed in the three tissues, and different tissues have different functions, but the oxytocin signaling pathway was widely enriched. To further explore the differences in the expression genes (DEGs) of HPO in different sheep breeds, we downloaded the transcriptome data in the public data, and the analysis of DEGs (Xinggao sheep vs. Sunite sheep in Hypothalamus, Xinggao sheep vs. Sunite sheep in Pituitary, and Xinggao sheep vs. Suffolk sheep in Ovary) revealed the neuroactive ligand-receptor interactions. In addition, the gene subsets of the transcription factors (TFs) of DEGs were identified. The results suggest that 51 TF genes and the homeobox TF may play an important role in transcriptional variation across the HPO. Altogether, our study provided the first fundamental resource to investigate the physiological functions and regulation mechanisms in sheep. This important data contributes to improving our understanding of the reproductive biology of sheep and isolating effecting molecular markers that can be used for genetic selection in sheep.

Keywords: HPO; reproductive trait; sheep breeding; transcription atlas.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Biomarkers
Female
Gene Expression Profiling*
Reproduction / genetics
Sheep / genetics
Sheep, Domestic* / genetics
Transcriptome / genetics

Substances

Biomarkers

Grants and funding

This research was funded by the Natural Science Foundation of Inner Mongolia Autonomous Region (No.2021ZD05), the Inner Mongolia Science and Technology Program (No.2021GG0008, No. 2021GG0012, No. 2019GG349), College of Animal Science, Inner Mongolia Agricultural University of High-level Achievement Cultivation Project (No. BZX202201), the Science and Technology Major Project of Inner Mongolia (No. 2020ZD0003, No. 2019ZD016), the National Key Research and Development Program of China (No. 2021YFD1200905), and the Modern Agricultural Industry Technology System of China (CARS-38).