The sheep genome illuminates biology of the rumen and lipid metabolism

Abstract

Sheep (Ovis aries) are a major source of meat, milk, and fiber in the form of wool and represent a distinct class of animals that have a specialized digestive organ, the rumen, that carries out the initial digestion of plant material. We have developed and analyzed a high-quality reference sheep genome and transcriptomes from 40 different tissues. We identified highly expressed genes encoding keratin cross-linking proteins associated with rumen evolution. We also identified genes involved in lipid metabolism that had been amplified and/or had altered tissue expression patterns. This may be in response to changes in the barrier lipids of the skin, an interaction between lipid metabolism and wool synthesis, and an increased role of volatile fatty acids in ruminants compared with nonruminant animals.

Fig. 1. The genome of sheep

(A) 1,097 segmental duplications (length >5 kb) in the two Texel sheep (). (B) Sheep vs. cattle chromosome break points (), gaps in Oar v3.1 are red, probable misassemblies in UMD 3.1 are yellow and probable true structural differences are blue. (C) Distribution of SNPs in the Texel ewe in 1Mb non-overlapping windows, range of values 1 to 4954. (D) Distribution of SNPs in the Texel ram in 1 Mb non-overlapping windows, range of values 3 to 5676. (E) Distribution of mono-allelically expressed SNPs in 500kb sliding windows, range of values 0 to 42 (). The scale is in Mb. Positions of loci discussed in the text are indicated.

Fig. 2. Sheep relative to human and livestock evolution

A phylogenetic tree generated using single-copy orthologous genes (). The origins (black) and amplifications (red) of genes discussed in the text are marked. The scale is in millions of years ago (Mya). Blue numbers on the nodes are the divergence time from present (Mya) and its confidence interval. Dates for major events in the evolution of grasses are from () and ().

Fig. 3. Epidermal Differentiation Complex (EDC) gene expression and sequence organization

(A) Expression levels of the genes in the EDC region in selected sheep tissues. The abomasum is equivalent to the stomach of a non-ruminant. Genes are ordered according to their genomic order, with pseudogenes omitted. Genes discussed in the text are highlighted. (B) Proposed evolution patterns of the core 15 amino acid repeat of predicted TCHHL2 proteins. (C) Maximum likelihood phylogenetic tree of PRD-SPRRII and SPRR2 proteins. For clarity three representative cattle sequences shown, Bootstrap values ≥50% (500 replicates) are shown.

Fig. 4. Proposed sheep skin lipid metabolic pathways and the expression of the MOGAT3 region

(A) Proposed sheep skin lipid metabolic pathways. The proposed non-membrane form of MOGAT3 is red; the membrane form of MOGAT2/3 is blue. The glycerol-3-phosphate and MOGAT pathways to DAG are in blue and red arrows respectively. Dashed lines represent transport or diffusion of products. (B) Expression of eight MOGAT3 genes in sheep skin (Gansu fine wool), and sheep omentum, white adipose and liver (Texel), goat skin (Shanbei Cashmere), and goat liver (Yunling Black).