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. 2019 Apr 2;20(1):261.
doi: 10.1186/s12864-019-5620-6.

Rapid evolution of a retro-transposable hotspot of ovine genome underlies the alteration of BMP2 expression and development of fat tails

Zhangyuan Pan  1   2 , Shengdi Li  3   4 , Qiuyue Liu  1 , Zhen Wang  3 , Zhengkui Zhou  1 , Ran Di  1 , Xuejiao An  1 , Benpeng Miao  3   4 , Xiangyu Wang  1 , Wenping Hu  1 , Xiaofei Guo  1 , Shenjin Lv  2 , Fukuan Li  2 , Guohui Ding  3   4 , Mingxing Chu  5 , Yixue Li  6   7
Affiliations

Rapid evolution of a retro-transposable hotspot of ovine genome underlies the alteration of BMP2 expression and development of fat tails

Zhangyuan Pan et al. BMC Genomics. .

Abstract

Background: Sheep have developed the ability to store fat in their tails, which is a unique way of reserving energy to survive a harsh environment. However, the mechanism underlying this adaptive trait remains largely unsolved.

Results: In the present study, we provide evidence for the genetic determinants of fat tails, based on whole genome sequences of 89 individual sheep. A genome-wide scan of selective sweep identified several candidate loci including a region at chromosome 13, a haplotype of which underwent rapid evolution and spread through fat-tailed populations in China and the Middle East. Sequence analysis revealed an inter-genic origin of this locus, which later became a hotspot of ruminant-specific retro-transposon named BovB. Additionally, the candidate locus was validated based on a fat- and thin-tailed cross population. The expression of an upstream gene BMP2 was differentially regulated between fat-tailed and thin-tailed individuals in tail adipose and several other tissue types.

Conclusions: Our findings suggest the fixation of fat tails in domestic sheep is caused by a selective sweep near a retro-transposable hotspot at chromosome 13, the diversity of which specifically affects the expression of BMP2. The present study has shed light onto the understanding of fat metabolism.

Keywords: BMP2; Evolution; Fat tail; Retro-transposable hotspot; Sheep.

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Conflict of interest statement

Ethics approval and consent to participate

All the experimental procedures mentioned in the present study were approved by the Science Research Department (in charge of animal welfare issue) of the Institute of Animal Sciences, Chinese Academy of Agricultural Sciences (IAS-CAAS) (Beijing, China). Ethical approval on animal survival was given by the animal ethics committee of IAS-CAAS (No. IASCAAS-AE-03, 12 December 2016). Consent was obtained from the owners of the animals used in this study.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Figures

Fig. 1
Fig. 1
Selective sweeps in Chinese fat-tailed sheep. a Phylogenetic structure of Chinese Mongolian breeds (fat-tailed; clade in blue), Chinese Tibetan breeds (thin-tailed; clade in red) and a European-origin breed (thin-tailed; clade in green). T, Tan; STH, Small Tail Han; CB, Cele Black; WZ, Wuzhumuqin; H, Hu; VT, Valley Tibetan; PT, Prairie Tibetan; OL, Oula; AM, Australian Merino. b Phenotypic features of individuals from PT breed (top) and STH breed (bottom). c Manhattan plot of selective sweep statistic LSBL over 26 ovine chromosomes
Fig. 2
Fig. 2
Evidence of selection in fat-tailed breeds at ovine chromosome 13. a A local plot of LSBL at ovine chromosome 13. b Other evidences of selection including pair-wise genetic differences dxy between lineages (TBS, Tibetan sheep; MGS, Mongolian sheep; EUS, European sheep), as well as intra-lineage heterozygosity HP. c A variant heatmap shows haplotypic structures of 89 sheep from our WGS dataset (MGS, TBS, EUS), 20 sheep from Iran (IROA) and 160 sheep from Morocco (MOOA). Colors denotes different genotypes at each bi-allelic variant site
Fig. 3
Fig. 3
Retro-transposable origin of gene LOC101117953. a Alignment between ovine sequences of LOC101117953 and PPP1CC. b Gene tree constructed based on sequences of PPP1CC and its retro-paralogs (r-PPP1CC) from different species. c Genomic alignment between sheep and cattle shows the insertion point of r-PPP1CC
Fig. 4
Fig. 4
Identification of retro-transposable events at IBH region. a Scheme for identifying retro-transposable events at IBH region, specifically from 48.5 to 49.5 Mb at chromosome 13. b A circular plot of ovine chromosomes and six retro-transposable events detected at IBH region. c Sliding-window-based densities of the RTE BovB, calculated from the prediction of functional repeats by RepeatMasker. d Comparison of RTE occupation between IBH and random genomic regions (n = 10). Error bars denotes standard deviations. e The positions and emergence time of six retro-copies estimated based on a cross-species comparison
Fig. 5
Fig. 5
Predictive power of candidate SNPs on tail phenotypes. Strength of association was tested between candidate SNPs (IBH SNP1, IBH SNP2, BMP2 SNP and PDGFD SNP) and tail phenotypes (length and width). Two IBH markers are in complete LD, therefore only one is showed. P values were calculated based on linear regressions after adjustment for age and sex (assuming an additive effect of single allele). A more complete analysis is in Additional file 1: Table S4
Fig. 6
Fig. 6
Gene expression difference between fat-tailed and thin-tailed sheep. a Comparison of gene expression level for BMP2 and HAO1 in 17 tissue types between TBS and MGS (n = 4 for each). **, student’s t test P value < 0.01; *, student’s t test P value < 0.05. b Validation of BMP2 expression in adipose and uterine tissues using additional samples (n = 8 for each)
Fig. 7
Fig. 7
Evolutionary trajectory of IBH region as a target of recent selection in fat-tailed sheep. The river of life summarizes from upstream to downstream the timings of several key events, which contributed to the evolution of IBH sequence, as well as its recent sweep in fat-tailed sheep
See this image and copyright information in PMC

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