- Assessing genomic diversity and signatures of selection in Jiaxian Red cattle using. - Using whole-genome sequencing (WGS) data of 30 animals from the core breeding farm, we investigated the genetic diversity, population structure and genomic regions under selection of Jiaxian Red cattle. - Furthermore, we used 131 published genomes of world-wide cattle to characterize the genomic variation of Jiaxian Red cattle.. - Results: The population structure analysis revealed that Jiaxian Red cattle harboured the ancestry with East Asian taurine (0.493), Chinese indicine (0.379), European taurine (0.095) and Indian indicine (0.033). - Three methods (nucleotide diversity, linkage disequilibrium decay and runs of homozygosity) implied the relatively high genomic diversity in Jiaxian Red cattle. - We used θπ , CLR, F ST and XP-EHH methods to look for the candidate signatures of positive selection in Jiaxian Red cattle. - Conclusion: We provide a comprehensive overview of sequence variations in Jiaxian Red cattle genomes. - Selection signatures were detected in genomic regions that are possibly related to economically important traits in Jiaxian Red cattle. - We observed a high level of genomic diversity and low inbreeding in Jiaxian Red cattle. - 22 Xinong Road, Yangling 712100, Shaanxi, China Full list of author information is available at the end of the article. - How- ever, there are a limited number of studies on the genomic variation of native cattle breeds in China, and even fewer reports have been reported from Jiaxian Red cattle [2, 7, 8].. - Jiaxian Red is an indigenous cattle breed in China, and it has been intensively bred for beef during over the past 30 years, leading to genetic improvement in production traits [9]. - In the early production practice, the local people mainly used the draught as the selection stand- ard, which led to the large body size of Jiaxian Red cat- tle. - For now, Jiaxian Red cattle have been evolved into a beef cattle breed with excellent meat quality, tough feed- ing resistance and high fertility [10]. - Previous studies have used various methods to study the genomic diver- sity and population structure of the Jiaxian Red cattle breed, e.g., mitochondrial, Y chromosome or autosomal data . - These studies indicated that Jiaxian Red originated from the crossbreeding between taurine and indicine cattle. - Studies attempting to explain the growth and meat quality of Jiaxian Red cattle have focused on single gene SNPs (single nucleotide polymorphisms), such as MYLK4 [13], TRPV1 and TRPA1 [14], and CRTC3 [15]. - To expand our knowledge of genomic variations and selective sweeps that may potentially have arisen as a re- sult of recent selection of Jiaxian Red, we performed whole-genome sequencing of 30 Jiaxian Red cattle and identified SNPs based on the Bos taurus reference gen- ome assembly (ARS-UCD1.2). - SNPs of Jiaxian Red were. - Individual genomes of 30 Jiaxian Red cattle were gener- ated to ~ 10.6 × coverage each and were jointly geno- typed with publicly available genomes of five “core”. - We annotated biallelic SNPs that were discovered in 30 Jiaxian Red cattle. - Functional annotation of the polymorphic sites revealed that the vast majority of SNPs were present either intergenic re- gions (59.2%) or intronic regions (37.8. - Exons con- tained 0.8% of the total SNPs with 70,165 non- synonymous SNPs and 112,847 synonymous SNPs (Table S3).. - Bos indicus ) displayed the highest number of SNP, followed by crossbred Jiaxian Red . - To explore relatedness among Jiaxian Red cattle and other cattle breeds distributed worldwide, we conducted ADMIXTURE, neighbor-joining (NJ) and principle com- ponent analysis (PCA) using genomic SNPs (Fig. - when K=4, the Jiaxian Red cattle showed clear evidence of genetic heterogeneity with shared genome ancestry with East Asian taurine (0.493), Chinese indicine (0.379), European taurine (0.095) and Indian indicine (0.033) genetic background (Fig. - The genetic influence of Bos indicus was greater on Jiaxian Red than that on. - The NJ tree and PCA ana- lysis provided similar results, with all the “core” cattle populations forming their own separate clusters, and Jiaxian Red as well as Qinchuan cattle are found at an intermediate position between Bos taurus and Bos indi- cus (Fig. - To evaluate the ROH pattern of Jiaxian Red and other cattle breeds, we divided the length of ROH into four size classes: 0.5–1 Mb, 1–2 Mb, 2-4 Mb, >. - The total lengths of ROHs in Mishima and European taurine breeds (Jersey, Here- ford, Angus and Simmental) are longer than those of Jiaxian Red because European commercial breeds have been artificially selected for a longer period of time (Fig. - 1 Population structure and relationships of Jiaxian Red in comparison to several possible ancestral breeds. - b Neighbor-joining tree of the relationships between the ten cattle breeds (161 animals). - Functional enrichment analysis of the specific SNPs in Jiaxian red. - When comparing the two Chinese cattle breeds, Jiaxian Red and Qinchuan cattle shared a relatively high number of SNPs ( n accounting for ~ 72% and ~ 88% of the total SNPs of Jiaxian Red and Qinchuan respectively, indicat- ing that the genetic relationship between the two cattle breeds is very close.. - In order to find out the genetic differences between Jiaxian Red and Qinchuan cattle, ANNOVAR software was used to identify the nonsynonymous SNPs (nsSNPs) of breeds. - in Jiaxian Red and Qinchuan breeds, respectively. - Finally, a total of 617 and 88 genes were identified in Jiaxian Red and Qinchuan. - 0.05) GO BP terms were enriched in Jiaxian Red (Figure S2 and Table S4). - that might contribute to the specific characteristics of the Jiaxian Red breed. - We applied the nucleotide diversity analysis (θπ) and the composite likelihood ratio (CLR) methods to detect gen- omic regions related to selection in Jiaxian Red breed.. - The only significant KEGG path- way in Jiaxian Red was “Regulation of actin cytoskeleton”. - Over- representation analysis of GO terms shows that Jiaxian Red has increased GO categories involved in cysteine- type endopeptidase inhibitor activity involved in apop- totic process ( TNFAIP8 , DPEP1 , SNCA. - F ST and XP-EHH test were also performed to detect the positive selection signatures between Jiaxian Red and the commercial breeds (Angus and Red Angus) (Fig. - of these, 238 genes were detected in both methods and 17 genes were potentially selected candi- date genes in Jiaxian Red (Table S12). - It’s worth noted that four overlapped genes ( POLR3B , RAB11FIP2 , RFX4 and SLAMF1 ) were detected among the 4 mentioned selec- tion methods, indicating that these genes were strongly selected in Jiaxian red cattle. - We ex- plored the population genetic structure of Jiaxian Red cat- tle in the context of the cattle breeds/populations with potential ancestors [2]. - 1a), the ancestral contributions of Jiaxian Red cattle came from East Asian taurine. - Jiaxian Red is closest related to the Qinchuan breed, both of which are located in the central area of China, but Jiaxian Red shared more Bos indicus ancestry.. - The nucleotide diversity of Jiaxian Red (mean θπ = 0.0029) was lower than that of Chinese indicine cattle (mean θπ but approximately two times higher than that of European breeds . - The relative high level of genomic diversity found in Jiaxian Red is likely the re- sults of hybridization with taurine and indicine, and may also reflect the weaker and shorter selection history.. - Jiaxian Red (mean θπ = 0.0029) and Qinchuan cattle (mean θπ = 0.0026) showed a similar level of nucleotide diversity (Fig. - We also analyzed the ROH distribution pattern of Jiaxian Red by comparing with other cattle breeds. - Our results showed that Jiaxian Red exhibits larger amounts of short/medium ROH (0.5 to 2 Mb) and the lowest quan- tities of average ROH in comparison to the cattle breeds analyzed in this study, which is consistent with the re- ported ROH patterns of other taurine-zebu hybrid breeds [17].. - In our analysis, Jiaxian Red and Qinchuan cattle showed a very close genetic relationship. - Genes related to the immunity and “Sensory perception” were enriched in Jiaxian Red, which reflects the adaptability of Jiaxian Red cattle to environment. - In addition, we also identified sig- nificant signatures of selective sweeps in Jiaxian Red breed. - Jiaxian Red has been intensively bred for beef during over the past 30 years, leading to the genetic im- provement in production traits, especially the. - Jiaxian Red genome showed signs of selection in some genes of the “Regulation of actin cytoskeleton”. - PPP1R12A has been reported to be one of the highly expressed genes in intramuscular adipose tissue in the. - 3 Analysis of the signatures of positive selection in the genome of Jiaxian Red. - a Manhattan plot of selective sweeps in Jiaxian Red. - and Tajima ’ s D plots of the SLAMF1 , CD84 and SLAMF6 genomic regions. - The major allele at each SNP position in Jiaxian Red is colored in yellow, the minor one in green. - pig [33], and it has also been found under positive selec- tion in Hanwoo (a famous beef cattle breed in Korea) [34], indicating that this gene may be related with meat marbling (intramuscular fat content) of Jiaxian Red (Fig.. - ROCK1 gene has been considered one of the candidate genes related to IMF under selection in Ankole cattle [5].. - When comparing the selection signatures of Jiaxian Red cattle with commercial breeds, two positively se- lected genes associated with muscle development ( PHAC TR1 and EYA3 ) and one gene ( CYB5R4 ) influencing the fatty acid metabolism have been identified in Jiaxian Red. - PHACTR1 is a member of the phosphatase and actin regulator family, which is involved in regulating the reorganization of the actin cytoskeleton. - This gene has also been reported as one of the can- didate genes for the QTL for oleic acid percentage in Japanese Black cattle [23], indicating that CYB5R4 may be related with meat tenderness of Jiaxian Red. - We detected positively selected gene CCSER1 in Jiaxian Red, which was reported to be associated with the growth and feed efficiency in beef cattle [26].. - We found a region on BTA Mbp containing three SLAMF (signaling lymphocytic activation molecule fam- ily) genes ( SLAMF1 , CD84 and SLAMF6 ) that showed a strong signal of positive selection in Jiaxian Red. - The positive selection signals around this region are further confirmed by significantly lower values of Tajima’s D and long haplotype patterns in Jiaxian Red (Fig. - may be one of the candidate regions of high disease re- sistance of Chinese native cattle, which may be useful as a genetic target for improving disease resistance in cattle breeding. - But the haplotype of Jiaxian Red in this region is obviously not fixed, and similar haplotype pattern ex- ists in Qinchuan cattle. - This further suggested that Jiax- ian red cattle did not experience the same intensive artificial selection as European cattle breeds. - In addition, two genes ( RFX4 , SRD5A2 ) associated with fertility [27, 28] displayed signals of positive selection in Jiaxian Red cattle. - These genes might be related to the strong repro- ductive performance of Jiaxian Red cattle.. - Jiaxian Red breed is a valuable and widely used genetic resource in local area due to its higher beef productivity and better adaptability. - With this regard, our results provide a basis for further research on the genomic characteristics of Jiaxian Red cattle in relation to economically important traits.. - This study provided a comprehensive overview of gen- omic variations in Jiaxian Red cattle by using WGS data.. - The characterization of population structure and gen- omic diversity will point out the direction for genetic as- sessment and development of reasonable breeding strategies of Jiaxian Red cattle. - Thirty blood samples of Jiaxian Red cattle were collected from the core breeding farm of Jiaxian Red Cattle Breed- ing Center (Table S1). - To explore the ancestry proportions of Jiaxian Red and compare the genetic diversity with worldwide cattle breeds, we collected additional 131 samples according to the five “core” groups proposed by Chen et al. - Genome scans for selection in Jiaxian Red cattle were per- formed using the following strategy. - First, we detect the se- lection signatures within Jiaxian Red cattle using two different statistics, the nucleotide diversity (θπ) and the composite likelihood ratio (CLR) [52]. - Empirical P values were calculated for π and CLR windows, and the overlap of the top 1% windows of each method were considered as candidate signatures of selection.. - Second, we performed comparisons between Jiaxian Red versus commercial cattle breeds (Angus and Red Angus) using fixation index ( F ST ) and cross-population extended haplotype homozygosity (XP-EHH). - An XP-EHH score is direc- tional: a positive score suggests that selection is likely to have happened in Jiaxian Red cattle, whereas a negative score suggests the same about reference population. - Size and color of the bubble represent amount of differentially expressed genes enriched in pathway and enrichment significance, respectively.. - List of additional cattle samples for analysis of genetic background in Jiaxian Red cattle. - 5 in Jiaxian Red cattle. - A summary of genes from θπ in Jiaxian Red. - A summary of genes from CLR in Jiaxian Red. - KEGG pathway analysis of Jiaxian Red candidate genes overlapped by θπ and CLR methods. - GO enrichment of Jiaxian Red candidate genes overlapped by θπ and CLR methods. - A summary of genes from XP-CLR in Jiaxian Red cattle. - A sum- mary of genes from F ST and XP-EHH in Jiaxian Red cattle. - Permission for blood sampling was obtained from the Jiaxian Red Cattle Breeding Center on site.. - Summary of the improvement work of breeding and conservation of Jiaxian red cattle (in Chinese). - Comprehensive analysis of the mitochondrial DNA diversity in Chinese cattle. - Whole-genome
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